Thermal stress impacts reproductive development and grain yield in rice

Plant Physiology and Biochemistry 115 (2017) 57e72

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Plant Physiology and Biochemistry journal homepage: www.elsevier.com/locate/plaphy

Review

Thermal stress impacts reproductive development and grain yield in rice Muhammad Shakeel Arshad a, Muhammad Farooq a, b, c, *, Folkard Asch b, Jagadish S.V. Krishna d, P.V. Vara Prasad d, Kadambot H.M. Siddique c a

Department of Agronomy, University of Agriculture, Faisalabad, Pakistan Institute of Agricultural Sciences in the Tropics, University of Hohenheim, 70599, Stuttgart, Germany The UWA Institute of Agriculture, The University of Western Australia, LB 5005, Perth, WA, 6001, Australia d Department of Agronomy, Kansas State University, Manhattan, KS, 66506, USA b c

a r t i c l e i n f o

a b s t r a c t

Article history: Received 2 January 2017 Received in revised form 10 March 2017 Accepted 14 March 2017 Available online 16 March 2017

Rice is highly sensitive to temperature stress (cold and heat), particularly during the reproductive and grain-filling stages. In this review, we discuss the effects of low- and high-temperature sensitivity in rice at various reproductive stages (from meiosis to grain development) and propose strategies for improving the tolerance of rice to terminal thermal stress. Cold stress impacts reproductive development through (i) delayed heading, due to its effect on anther respiration, which increases sucrose accumulation, protein denaturation and asparagine levels, and decreases proline accumulation, (ii) pollen sterility owing to tapetal hypertrophy and related nutrient imbalances, (iii) reduced activity of cell wall bound invertase in the tapetum of rice anthers, (iv) impaired fertilization due to inhibited anther dehiscence, stigma receptivity and ability of the pollen tube to germinate through the style towards the ovary, and (v) floret sterility, which increases grain abortion, restricts grain size, and thus reduces grain yield. Heat stress affects grain formation and development through (i) poor anther dehiscence due to restricted closure of the locules, leading to reduced pollen dispersal and fewer pollen on the stigma, (ii) changes in pollen proteins resulting in significant reductions in pollen viability and pollen tube growth, leading to spikelet sterility, (iii) delay in heading, (iv) reduced starch biosynthesis in developing grain, which reduces starch accumulation, (v) increased chalkiness of grain with irregular and round-shaped starch granules, and (vi) a shortened grain-filling period resulting in low grain weight. However, physiological and biotechnological tools, along with integrated management and adaptation options, as well as conventional breeding, can help to develop new rice genotypes possessing better grain yield under thermal stress during reproductive and grain-filling phases. © 2017 Elsevier Masson SAS. All rights reserved.

Keywords: Anther dehiscence Pollen sterility Productivity Reproductive and grain-filling stages Rice Thermal stress Tolerance

Contents 1. 2.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 58 Impact of thermal stress on reproductive processes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 59 2.1. Cold stress . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 59 2.1.1. Flower initiation and development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 59 2.1.2. Gametophyte development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 59 2.1.3. Pollen development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 59 2.1.4. Anthesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61 2.1.5. Pollination and fertilization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61 2.2. Heat stress . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61

* Corresponding author. Department of Agronomy, University of Agriculture, Faisalabad, Pakistan. E-mail address: [email protected] (M. Farooq). http://dx.doi.org/10.1016/j.plaphy.2017.03.011 0981-9428/© 2017 Elsevier Masson SAS. All rights reserved.

58

3.

4.

5. 6.

M.S. Arshad et al. / Plant Physiology and Biochemistry 115 (2017) 57e72

2.2.1. Flower initiation and development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61 2.2.2. Gametophyte development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61 2.2.3. Pollen development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61 2.2.4. Anthesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 64 2.2.5. Pollination and fertilization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 64 Grain development and yield formation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 64 3.1. Cold stress . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 64 3.1.1. Starch and protein synthesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 64 3.1.2. Rate and duration of grain filling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 65 3.1.3. Carbohydrate supply and grain growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 65 3.1.4. Hormonal imbalances during grain filling and maturation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 65 3.2. Heat stress . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 65 3.2.1. Starch and protein synthesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 65 3.2.2. Rate and duration of grain filling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 65 3.2.3. Carbohydrate supply and grain growth . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 66 3.2.4. Hormonal imbalances during grain filling and maturation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 66 Strategies to improve tolerance against thermal stress . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 66 4.1. Cold stress . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 66 4.1.1. Selection and breeding . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 66 4.1.2. Marker-assisted selection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 66 4.1.3. Genetic engineering . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 68 4.2. Heat stress . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 69 4.2.1. Selection and breeding . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 69 4.2.2. Marker-assisted selection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 69 4.2.3. Genetic engineering . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 69 Management strategies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 69 Conclusion and future research thrusts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 70 Contribution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 70 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 70

1. Introduction Rice (Oryza sativa L.) is a most important staple cereal crop with about half of the world population depending on it for their dietary requirements. Worldwide, rice is grown in 114 countries on 161 million hectares (M ha) to produce >650 million tons (FAO, 2012). In the Asia-Pacific region, rice is grown from the flood plains of Bangladesh to the Himalayan foothills of Nepal, and from the rainforests of Indonesia to the desert plains of Australia. Over 90% of the global rice, is produced and consumed in Asia, on an area of 143 M ha to produce 612 million tons (FAO, 2012). The productivity of rice in the tropics, subtropics and temperate areas is threatened due to frequent episodes of low (cold stress) and high (heat stress) temperatures (Table 1). A recent report projected that the occurrence of extreme temperature stress will increase in the future (IPCC, 2014). All plant species have an optimum temperature range for efficient physiological functions such as growth, development and reproduction. Temperatures above or below that range will have a negative impact on plant performance leading to a loss in economic yield. Chilling and freezing stresses are collectively known as lowtemperature stress or cold stress. Chilling stress is induced when temperatures are below optimum and low enough to cause injury without producing ice crystals within the soft tissues of the plants; freezing stress arises when crystals of ice come into existence inside the soft tissues. Tolerance capabilities vary among different plants for chilling (0e15
C) and freezing (<0
C) temperatures. Rice originated from the tropical and subtropical regions, that's why it is highly sensitive to cold stress as well as its production is also severely affected in temperate regions leading to complete crop failure in extreme cases (Xie et al., 2012). The incidence of cold stress is common in many Asian countries (Koike et al., 1990; Zhang et al., 2014a,b). In other regions, such as West and East Africa,

United States, Europe, and South America, rice crops must be cold tolerant as the frequent occurrence of chilling stress threatens its productivity. The southernmost state of Brazil (Rio Grande do Sul), produces >60% of the total rice production in South America and is prone to low temperatures. This region, along with Argentina and Uruguay, is prevalent for the cultivation of indica rice in South America. The physiological causes of yield losses in rice from cold stress vary between vegetative and reproductive stage. During the vegetative stage, source build-up can be a severe constraint whereas in the reproductive stages cold stress affects the sink formation through e.g., floral abscission, sterile pollen production, pollen tube burst, aborted ovules, as well as abridged seed development (Kuroki et al., 2007; Oliver et al., 2007). Temperatures above the optimum range for plant growth and development, defined as heat stress, can equally injure or permanently damage both vegetative and generative organs of rice. The impact of heat stress on plant performance primarily depends on the intensity, duration, and timing (relative to plant development) of the stress, but is more detrimental during the reproductive and grain-filling stages (Cao et al., 2008; Tenorio et al., 2013). Yield losses due to heat stress, induced by temperatures >33
C, are common in several parts of the world (Table 1). IPCC projects a mean annual temperature increase of 0.7e0.9
C per decade in Southeast Asia (IPCC, 2014) which equates to 4.8
C by 2100 (ADB, 2009). Every 1
C rise in to minimum seasonal growing temperature may reduce grain yield by about 10% (Peng et al., 2004, Table 1). Recent reviews on the impact of cold (Zhang et al., 2014b), and heat stress on rice (Mitsui et al., 2013), focused primarily on vegetative processes and grain yield. These reviews illustrated limited facts about the consequences of cold and heat stress on the reproductive processesdthe most sensitive to adverse thermal environmentsdincluding panicle formation, flowering,

M.S. Arshad et al. / Plant Physiology and Biochemistry 115 (2017) 57e72

59

Table 1 The influence of thermal stress during the reproductive stage of rice on grain yield. Stress type

Growth stage

Temperature

Yield reduction (%)

Country/Region

References

Cold stress

Flowering

13
C for 15 days (tolerant variety) 13
C for 15 days (sensitive variety) 13
C for 150 days 13
C for 150 days 1
C increase in minimum temperature Average daily temperature above 30
C for 15 days Tolerant variety with mean daytime temperature above 33
C Tolerant variety with mean daytime temperature above 33
C Sensitive variety with mean daytime temperature above 33
C Sensitive variety with mean daytime temperature above 33
C

19%

Iran

Ghadirnezhad and Fallah, 2014

29%

Iran

Ghadirnezhad and Fallah, 2014

26% 9.2% 10%

Korea Korea IRRI-Philippines

Lee, 2001 Lee, 2001 Peng et al., 2004

20e30%

China

Zheng et al., 2005

5.6e14.6%

China

Cao et al., 2009

3.9e9.2%

China

Cao et al., 2009

24.4e27.5%

China

Cao et al., 2009

6.6e13.0%

China

Cao et al., 2009

Flowering

Heat stress

Reproductive and grain filling Reproductive and grain filling Growing season Heading

Heading

Early grain filling

Heading stage

Early grain filling

fertilization, grain formation and grain yield. In this review manuscript, the effects of cold and heat stresses on rice reproductive physiology are discussed, and opportunities and strategies for improving rice tolerance to cold and heat stress are described.

2. Impact of thermal stress on reproductive processes Abiotic stresses can influence crop performance at any stage of development, but the reproductive phase is the most sensitive in this regard (Andaya and Mackill, 2003; Jagadish et al., 2007; Fu et al., 2008). The reproductive phase spans panicle initiation through to physiological grain maturity. This section summarizes and discusses current knowledge about the impact of cold and heat stresses on flower initiation and development, gametophyte development, pollen development, flowering and anthesis, pollination and fertilization, the grain filling phase and its speed, and grain yield.

2.1. Cold stress 2.1.1. Flower initiation and development Rice is a short-day plant without any vernalization requirements; since it grows mainly in tropical regions, it is more likely to suffer from chilling stress than from freezing stress especially during floral development (Lu et al., 1999; Kuroki et al., 2007). Panicle initiation is strongly influenced by thermal environments prior to the reproductive stage, as rice needs to accumulate varietyspecific heat sums (degree days) before the reproductive stage can be initiated (Shrestha et al., 2013). Thus, low temperatures alone, or in combination with non-inductive photoperiods, will delay panicle initiation and subsequent flowering (Shrestha et al., 2013). At the booting stage, cold stress inhibits pollen growth, which affects spikelet fertility (Table 2). Often, entire panicle branches are aborted before flowering due to ovule abortion (Fig. 1).

2.1.2. Gametophyte development Haploid gametophytes are produced from the diploid cells by meiosis in higher plants. Male organ sensitivity toward thermal stress, considerably increases after the onset of meiosis (Oliver et al., 2005). Cold stress causes protein denaturation in the anthers at the tri-nucleate step of the early development stage of microspores in rice, which results in substantial pollen infertility (Oliver et al., 2005). At the meiotic stage, anther respiration declines with declining temperature resulting in sucrose accumulation in the anther, protein degradation, altered composition of amino acids, and reduced proline and increased asparagine concentrations (Mamun et al., 2006). Chilling stress interferes with the formation of the microspore wall in rice plants (Mamun et al., 2006). A callose wall is formed just before meiosis, which surrounds the dyads and tetrads (microspore mother cells). This callose wall is critical in the formation of the microspore wall. In rice, one of the leading causes of pollen barrenness under chilling stress is the early termination of callose wall, which conceals the segregating microspores involved in late meiosis, and consequent poor growth of wall in the resulting microspores (Fig. 2; Mamun et al., 2006). Primary growth of the microspore is very sensitive to chilling in rice (Mamun et al., 2006). Little is acknowledged for the effects of cold stress at panicle initiation on the female organs in rice. Since the macrospore and its early development constitute at least 50 percent of the reproductive process, we suggest that future research efforts investigate the effects of low temperature on female flower development in rice.

2.1.3. Pollen development Pollen development occurs within the anther where an initial cellda sporogenous cell known as pollen mother celldundergoes meiosis for tetrad formation. This phase is known as microsporogenesis, and through the action of a combination of enzymes released by the tapetum, ends with the release of unicellular microspores from the tetrads (Fig. 2). Through pollen mitosis I (PM-I), which is a highly asymmetric cell division, the released

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Table 2 The influence of thermal stress on reproductive development in rice. Stress type Trait

Experimental conditions

Day temperature (
C) Night temperature (
C) Impact

References

Cold stress Spikelet fertility Floret fertility Spikelet fertility Pollen viability Spikelet fertility Heat stress Days to flowering Flowering time (day)

Sunlit phytotron Field e e Field TGC Growth cabinets

12 e 19.6 16 15 30.4 and 39.7 29.6, 33.7, and 36.2

e <18 e e e 21.2 and 22.1 e

Satake et al., 1987 Godwin et al., 1994 Lu et al., 1999 Gothandam et al., 2007 Dingkuhn et al., 2015 Oh-e et al., 2007 Jagadish et al., 2008

Sunlit phytotron e e TGC

34e39 e 28 and > 35 Ambient þ 5

e e e e

Pollen viability

TGC

Ambient þ 5

e

Pollen fertility

Phytotron

32 and 39

e

Pollen sterility Pollen diameter

Greenhouse Sunlit phytotron

40 and 30 34e39

21 and 21 e

Thecae dehiscence Pollination Pollination Pollination Pollination Pollination

Sunlit phytotron Sunlit phytotron e e Growth chamber TGC

34e39 34e39 e 28 and > 35 35 Ambient þ 5

e e e e e e

Pollen germination Pollen germination Pollen germination Spikelet fertilization rate Seed setting rate

e e Phytotron Greenhouse Greenhouse

e 28 and > 35 32 and 39 40 and 30 40e42

e e e 21 and 21 e

Spikelet tissue temperature Growth chambers Spikelet fertility Sunlit phytotrons

29.6e36.2 37.5

e 26

Spikelet fertility

Temperature Gradient Greenhouse

33

27

Spikelet sterility Spikelet fertility

TGC e

37 39

e 30

Pollen Pollen Pollen Pollen

production production production production

Negative Negative Negative Negative Negative Negative Average spikelet fertility was 84.0, 78.9, and 47.1% respectively Negative Negative Negative Average decrease in pollen production was 51% Average decrease in pollen viability was 91 to 75% Reduced pollen activity and pollen germination 5.9%e28.2% Decreased by 2.9% and 4.3% Negative Negative Negative Negative Negative Average reduction in the number of pollen on the stigma was 43% Negative Negative Negative Negative Infertile grain rates were 11.2%e25.3% Negative Reduced fertility (seed set) Average decrease was from 74 to 38% and from 76 to 37% 10% Fertility totally lost

Matsui et al., 2000 Xu et al., 2001 Li et al., 2002 Prasad et al., 2006

Prasad et al., 2006

Tang et al., 2008

Cao et al., 2009 Matsui et al., 2000 Matsui et al., 2000 Matsui et al., 2000 Xu et al., 2001 Li et al., 2002 Morokuma and Yasuda, 2004 Prasad et al., 2006

Xu et al., 2001 Li et al., 2002 Tang et al., 2008 Cao et al., 2009 Fu et al., 2008 Jagadish et al., 2007 Matsui and Omasa, 2002 Prasad et al., 2006

Oh-e et al., 2007 Endo et al., 2009

TGC, temperature gradient chamber.

microspores undergo microgametogenesis, to generate bicellular pollens from germ and somatic cells. After PM-I, pollen mitosis II (PM-II) occurs for the development of twin spermatozoa from further mitotic division of germ cells. PM-II timing differs with plant species, occasionally taking place inside the anthers, typically throughout the growing pollen tube. A nutritive sporophytic layer of cells known as the tapetum surrounds the pollen mother cells in the locule. Tapetum is the most important in nutrient supply to emerging microspores and pollen grains. Typically, in rice, the tapetum is the deepest layer of anther wall hypertrophy. The regulation of pollen development is controlled by gametophytic (microspore/pollen) and sporophytic (tapetum) genetic expressions (Fig. 2). Although cold stress affects both male and female reproductive development in rice, however, the male organ is more sensitive as compared to female organ (Koike et al., 1990). Chilling stress affected the young microspores during the pollen growth (Fig. 2) such that mid-season, cool temperatures are the main environmental constraint for rice cultivation in temperate areas and the Tropics at high elevations (Andaya and Mackill, 2003). Cold stress

causes pollen sterility due to disruption in the meiotic phase of pollen development (Fig. 2). Under cold stress, anthers display irregular hypertrophy and vacuolation of the tapetum, an unusual accumulation of starch in the plastids, the early breakdown of callose (1,3-b-glucan), and poor pollen tube development. However, development of the tapetum is the main point of sensitivity under cold stress (Gothandam et al., 2007). Cold stress prevents involuntary action of tapetum cell death, reduces invertase levels in the tapetum wall, as well as prevents successful transport of the desired amount of hexose sugars to the tapetum (Gothandam et al., 2007), all evidence that cold stress restricts tapetum functioning. Starvation of the developing microspores takes place due to the lower levels of glucose, sucrose and fructose, thus infertile pollen production occurs (Fig. 2). Under cold stress, pollen sterility is caused by the interruption of cell wall bound acid invertase activity within the tapetum, which restricts starch accumulation in the pollen (Oliver et al., 2005). Therefore, cold stress inhibits sucrose supply, restricts pollen development, and permanently disrupts pollen (Oliver et al., 2005). In addition, during cold stress, hexose can accumulate in anthers

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to cold stress. Under cold stress, development of the tapetum is the major site of sensitivity. Cold stress interrupts tapetum functioning; anthers show irregular hypertrophy, vacuolation of the tapetum, unusual starch accumulation in the plastids, early breakdown of callose, and poor development of pollen tubes. A reduction in the supply of sugars leads to starvation in the developing microspores and, thus, the pollen sterility. Early anthesis is very sensitive to cold stress and leads to spikelet sterility. 2.2. Heat stress

Fig. 1. The influence of cold stress on panicle branches before flowering.

during the early binucleate stage or young microspore stage, reducing the sucrose/hexose quotient (Oliver et al., 2005). Increase in the abscisic acid (ABA) level, due to cold stress, is also involved in pollen sterility (Oliver et al., 2007). The mechanisms of pollen sterility induced by cold stress are not well understood in rice, but cold-tolerant rice plants accumulate very low levels of ABA in anthers to sustain carbohydrate metabolism for microspore development (Oliver et al., 2005). 2.1.4. Anthesis In rice, anthesis phase is the most critical under cold stress as it includes critical events such as flower opening and anther dehiscence. Cold stress during anthesis causes spikelet sterility in rice, and possibly spikelet abortion and partial panicle exertion (Koike et al., 1990; Suh et al., 2010). The duration of the chilling stress is a major factor determining the extent of the injury. Floral structures in rice are relatively more tolerant to cold stress during the first three days of anthesis. However, after five days, a gradual decline takes place in the spikelet fertility leading to spikelet sterility (Takeuchi et al., 2001). 2.1.5. Pollination and fertilization In rice, reproduction takes place inside the spikelet, which contains the male (stamens) and female (pistils) reproductive organs surrounded by two protecting glumes. During anthesis, pollen shedding from the anthers to stigma occurs, following the germination of pollen grains and growth of pollen tube, leading to fertilization and grain development (Fig. 2). Rice plants grown under cold stress showed cytological as well as histological deviations, more so in the anthers as compared to pistils and other floral parts. However, artificial pollination with healthy pollens can overcome the cold damage (Hirano and Sano, 1998; Oliver et al., 2007). In summary, flower initiation events are adversely affected by cold stress. Cold stress negatively affects meiosis during booting and results in pollen infertility and ovule sterility. Often, entire panicle branches abort before flowering due to the ovule abortion (Fig. 1). During the meiotic stage, anther respiration is disrupted by low temperatures, which leads to secondary problems such as sucrose accumulation, protein degradation, altered composition of amino acids, reduced proline levels and increased asparagine levels. The early development of microspores is the most sensitive

2.2.1. Flower initiation and development The booting (when the flag leaf sheath is swollen) and heading (panicle emergence, anthers not yet visible) stages are highly sensitive to heat stress (Table 2; Fig. 3). Heat stress during the heading stage can restrict the swelling of pollen grains. A decline in floral reproduction can occur after only a few hours of heat stress during anthesis due to embryo abortion (Matsui et al., 2000). Under heat stress, deformed floral organs appear along with a reduction in number and size (Cao et al., 2008). Anther characteristics (number of cell layers, length, width, and length  width) are linked to fertility of pollens in japonica genotypes under the high temperature at 37.5/26
C (day/night), during anthesis (Table 2; Matsui and Omasa, 2002). Anther cell layers comprise (i) the septum, a partition that separates the locules of the anther and (ii) the tapetum, a nutritive sporophytic layer of cells which surrounds the pollen mother cells lying in the loculedthe chamber of the anther. As the tapetum have pivotal importance in the nutrient supply towards emerging microspores and pollen, that's why it keeps the two adjacent locules closed as a result of inhibited nutrition and growth. Under optimal conditions, the cell layers rupture for anther dehiscence to occur, but this does not take place under heat stress (Fig. 3). Heat stress reduces pollen fertility due to delayed locule opening since the locules are tightly closed as a result of the restricted rupture of cell layers (Fig. 3). Different layers of the anther separate the locule from lacuna between the septum layers. However, stomium (region of anther where dehiscence occurs) is associated with fertility under heat stress more than anther size (Matsui and Omasa, 2002). 2.2.2. Gametophyte development Heat stress causes tapetum degeneration and pollen sterility, particularly in the developing anthers during the early microspore stage in rice (Endo et al., 2009). Callose is an indicator of sterile ovules; its deposition at the end of the ovule chalaza is often used to evaluate early ovule degeneration (Endo et al., 2009). The pistil is sporophytic maternal tissue, which supports the developing gametophytes by providing nutrition. Generally, the male stamens are less sensitive to high temperature than the female pistils (Endo et al., 2009). However, there are limited facts which may prove the sensitivity of pistil to varying degrees of temperature. 2.2.3. Pollen development Heat stress disturbs a number of tapetum functions required for anther dehiscence and pollen germination on the stigma in rice (Endo et al., 2009). Heat stress reduces pollen viability and germination due to reduced uptake of iron by pollen tubes or microspores (Jagadish et al., 2010). Heat stress induces both quantitative and qualitative modifications in pollen proteins in different rice genotypes, which may lead to the loss of pollen viability and spikelet sterility (Das et al., 2014). Poor pollen development may increase spikelet sterility (Jagadish et al., 2010). In rice, after the first mitotic division of microspores, starch deposition takes place in pollen grain, and the number of starchcontaining pollen grain reduces in response to heat stress.

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Fig. 2. Influence of cold stress on reproductive development in rice. A. Starvation of microsporocyte: Cold stress reduces invertase levels in the tapetal cell wall and hexose sugars fail to reach the tapetum; hence, starvation of developing microspores takes place due to lower levels of glucose, sucrose and fructose, which leads to pollen sterility; B. Sterile pollen production and disruption of pollen grain: Cold stress induces pollen sterility due to irregular sugar metabolism in the tapetum and poor starch accumulation in pollen. Cold stress causes sucrose accumulation in anthers which leads to less sucrose supply to microspores due to sucrose conversion into glucose and fructose by cell wall bound invertase, which inhibits sucrose supply thereby limiting pollen development and resulting in permanent pollen disruption; C: Anther indehiscence: Due to the reduced metabolic rate of sugars under cold stress, pollen grain remain in the loculi of anthers; D. Immature pollen production and poor pollen shedding: Poor pollen viability and little or no pollen shedding on stigma due to reduced metabolic rate of sugars; E: Low pollen germination on stigma: Pollen fails to germinate on stigma due to low viability and reduced sugar metabolism.

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Fig. 3. The influence of heat stress on reproductive development in rice. A: Tapetum degeneration: Heat stress causes major alterations in the genetic expression which causes tapetum degeneration. Certain genes control tapetum activity at the microspore stage in immature anthers; B: Poor and sterile pollen production: Reduced cell division of the microspore mother cells reduces pollen production. Pollen grain abortion, at early mitosis, is caused by tapetum disintegration and programmed cell death by the reduced activity of invertase enzyme in the tapetum. Pollen sterility is caused by major alterations in pollen proteins and gene expression; C: Poor anther dehiscence: Mainly caused by alterations in pollen proteins under heat stress and partial closure of locules; D: Less pollen shedding: Heat stress causes limited closure of locules resulting in reduced pollen dispersal; E: Poor pollen germination on stigma: Due to irregular dehiscence of anthers and fewer pollen to germinate on the stigma; F: Poor pollen tube development: Mainly due to alterations in pollen proteins.

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Negative impact of high temperature on the production of pollen is ascribed to reduced meiocyte division, and poor development of microspores (Cao et al., 2008). Pollen grain produced by anthers are directly associated with the original number of meiocytes. The abortion of pollen before mitosis is caused by early tapetum disintegration and programmed cell death, and/or reduced activity of the invertase enzyme in the tapetum (Ku et al., 2003). Proteomics of heat tolerant and sensitive rice anthers at high and optimal temperature conditions did not show alterations in the expression of invertases (Jagadish et al., 2010). Heat stress alters some characters of reproductive structures such as enlarged pores in anthers, and reduced stigma length, pollen number, and protein expression in anthers (Jagadish et al., 2010). The growth of outer layers in the wall of anther, like epidermis, endothecium, septum, as well as stomium, can be disturbed by heat stress (Matsui and Omasa, 2002) and cause anther indehiscence (Fig. 3). Pollen protein content and viability and decrease under heat stress. Cell membranes are mainly comprised of proteins and lipids, which are disintegrated under heat stress, disturbing the structure and integrity of the membrane and significantly reducing pollen viability (Das et al., 2014). Heat stress before flowering reduced pollen viability and, therefore, spikelet fertility (Fig. 3; Das et al., 2014). The water contents of pollen are essential for the production as well as dispersion of pollen grains. During the landing of pollen grain on a well-suited stigma, the water content is modified as per environmental fluctuations (Das et al., 2014). Non-reducing sugars, such as sucrose, are needed when pollen experiences a reduction in cell water content. Under high water content, these sugars work as compatible solutes, but when water is lost, the sugar molecules act as substitutes of H2O molecules at the hydrogen bonding site for the preservation of inherent assembly of proteins as well as space among phospholipids. The effect of heat stress varies among rice genotypes with regard to, for example, the water and carbohydrate content of pollen. These variations can be inherent due to a micro-environment impact of plants at the pollen development stage (Das et al., 2014).

2.2.4. Anthesis Heat stress at anthesis significantly reduces anther dehiscence (Fig. 3). For instance, an episode of high temperature (39
C and above) one day before flowering caused anther indehiscence (Matsui and Omasa, 2002). In rice, anthesis is the critical phase under heat stress (Prasad et al., 2006; Jagadish et al., 2007). The sensitive events of anthesisdanther dehiscence, pollination, pollen germination and pollen tube growthdare affected within 45 min of spikelet opening (Prasad et al., 2006). Poor seed set results from the suppressive effects of heat stress just before or during anthesis in rice (Table 2; Prasad et al., 2006). For instance, temperatures >35
C at anthesis for five days resulted in sterile spikelets and complete failure of seed production and for >1 h caused high sterility (Jagadish et al., 2007). Among different adaptation strategies, for the predicted extremely capricious climate, is to increase tolerance to heat stress at the most sensitive anthesis stage in rice. Tolerance typically consists of escape elements, e.g., a number of rice cultivars can adapt escape or avoidance mechanism to cope with heat stress at anthesis through macro-escape (heading within nonchalant growing period), micro-escape (anthesis at early hours in the morning), otherwise make canopy cool through effective transpiration (Jagadish et al., 2008). Spikelet sterility declined with early morning flowering under heat stress by completing flower opening before temperatures reached 35
C, a general threshold value for spikelet sterility (Jagadish et al., 2008).

2.2.5. Pollination and fertilization Rice can tolerate a narrow range of temperatures, particularly during flowering, fertilization, and grain development; heat stress will impair these stages and reduce grain yield. Pollination is a temperature-sensitive process with heat stress during flowering impeding pollen germination (Table 2; Fig. 3; Matsui et al., 2000). Factors contributing to pollination (pollen viability, reception, and germination) play a leading role in crop production. Heat stress adversely affects pre-zygotic and post-zygotic reproductive development more than vegetative development, and pre-fertilization development is more sensitive than postfertilization development (Cao et al., 2008). Consequently, male reproductive development and pre-fertilization development act as potential bottlenecks in the reproduction of plants during temperature stress (Jagadish et al., 2010). Male reproductive development in rice is recognized as highly sensitive to high temperature. Heat stress during flowering significantly reduces pollen production and the shedding of pollen grain (Prasad et al., 2006). Heat stress restricts the swelling of pollen grain, inhibits anther dehiscence and reduces pollen grain release (Fig. 3); as a result, fewer pollen are available for stigma interception (Fig. 3). Fertility is positively associated with the shedding of pollen grain on the stigma during both ambient and high temperatures. Reduced cell division of the microspore mother cells may reduce pollen production under heat stress (Fig. 3). Likewise, heat stress during or immediately after anthesis results in poor germination of pollen and stunted pollen tube growth (Fig. 3; Tang et al., 2008). Pollen grain exposure to heat stress can render pollen sterile within 10 min. To ensure successful fertilization, more than ten pollen grains need to germinate on stigma (Jagadish et al., 2010). In summary, heat stress at flower initiation leads to poor anther dehiscence which results in sterile spikelets. Heat stress may also disturb tapetum functions required for anther dehiscence and germination on the stigma. Heat stress for a short period during anthesis may cause spikelet sterility due to abridged anther dehiscence, reduced pollination, poor germination of pollen grains as well as restricted pollen tube development. Tolerance typically consists of escape elements, such as macro-escape and microescape. Heat stress delays flowering; in rice, heat stress affects pre-fertilization development more than post-fertilization development, and male reproductive development more than female reproductive development. Heat stress during flowering reduces the production of pollen and their shedding on the stigma, resulting in unfertilized florets and, thus severe loss of grain yield. However, it is unknown whether pollen abortion occurs during meiosis or mitosis or when starch accumulation is restricted. 3. Grain development and yield formation The main reason for low rice yields under thermal stress is poor grain development due to delayed flowering and inferior spikelets (Table 2). Poor grain development is attributed to a restricted carbohydrate supply, but this may not be the only reason because the grain has ample sucrose during early grain-filling. The poor performance of vital enzymes involved in carbon metabolism also contributes to poor grain development. In this section, starch and protein synthesis in grain, and the rate and duration of grain filling under cold and heat stress are discussed. 3.1. Cold stress 3.1.1. Starch and protein synthesis Increase or decrease in amylose concentration primarily depend upon the particular rice cultivar, but low temperature produce more amylose within the same cultivar than those under heat stress

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(Ahmed et al., 2008). Cold stress increased the amylose concentration in the grains of non-waxy japonica genotypes. Grain development at 15e20
C augmented the action of granule-bound starch synthase and amylose contents in several japonica rice cultivars (Hirano and Sano, 1998). 3.1.2. Rate and duration of grain filling Cold stress during grain development results in late and partial maturation of grain (Oliver et al., 2007). Grain development is regulated via sourceesink relationship, which is affected by temperature. Grain filling rate and period declined and grain abortion enhanced which also leads to undersized grains under cold stress (Saito et al., 2001; Oliver et al., 2007). 3.1.3. Carbohydrate supply and grain growth Cold stress reduces carbon exchange and photosynthetic rates along with the maximum quantum efficiency, and interrupts the main constituents of photosynthesis, such as the electron transport chain of the thylakoid membrane, the carbon reduction phase and stomatal conductance regulation. During phloem unloading, sucrose cleavage takes place for grain development mainly due to cell wall bound invertase activity; cleaving products break down to develop sink demand for the extra sucrose, and hexoses are delivered towards swiftly-growing cells (Hirose et al., 2002). 3.1.4. Hormonal imbalances during grain filling and maturation During grain development; carbohydrates, lipids as well as proteins accumulate within emerging grain. Grain development is mainly regulated by plant hormones such as cytokinins (CTKs) and ABA (Oliver et al., 2005, 2007). Plant hormones (auxins, gibberellins (GA) and ABA) regulated the grain filling through facilitating cell division, elongating endosperm, as well as by controlling the rate and translocation of photo-assimilates towards sink (Oliver et al., 2005, 2007). ABA also regulates the intrinsic cell death of tapetum cells (Ku et al., 2003). Under cold stress, ABA modulates the transitory enhancement of the ABA level in plants (Oliver et al., 2007), which indicates its significance as a regulator in response to stress. Stomatal closure occurs due to increased leaf ABA, which restricts photosynthesis due to low CO2 levels within the cells. In summary, cold stress in rice increases the grain amylose concentration, and reduces rate and duration of grain filling which increase grain abortion and the production of shriveled grain. Cold stress inhibits the supply of sucrose, restricts pollen development, and causes permanent failure of pollen. Cold stress reduces cell wall bound invertase activity in anthers tapetum in rice. Grain development is mainly regulated by plant hormones such as CTK and ABA. Under cold stress, the ABA concentration increases in plants, which indicates its significance as a regulator in the response to stress. 3.2. Heat stress 3.2.1. Starch and protein synthesis Rice cultivation is very sensitive to rising temperatures (Peng et al., 2004), as well as current temperature ranges are also forthcoming critical values for grain filling in numerous rice-producing regions (Umemoto et al., 1995). Fluctuation in the ambient temperature during grain filling disturbs starch accumulation (Umemoto et al., 1995), and the proportion of amylose to amylopectin in endosperm of rice (Ahmed et al., 2008). Heat stress affects grain filling by inhibiting the accumulation of starch (Ito et al., 2009) which constitutes the major component of the grain, making up 60e70% of its total weight. As the enzymatic

65

activities regarding starch synthesis are highly sensitive to high temperatures, heat stress influences grain filling by disturbing the associated enzymes (Oh-e et al., 2007). Several enzymes in the endosperm are reportedly involved in starch synthesis from sucrose including sucrose synthase (SuSy, EC 2.4.1.13), soluble starch synthase (SSS, EC 2.4.1.21), starch phosphorylase (SPase, EC 2.4.1.1), starch branching enzyme (SBE, EC 2.4.1.18), ADP-glucose pyrophosphorylase (AGPase, EC 2.7.7.27), and Granule-bound starch synthase (GBSS, EC:2.4.1.242). In a transcriptomic study under heat stress, several starch-synthesizing enzymesdsuch as GBSS and branching enzymes, particularly BEIIb, and a cytosolic pyruvate orthophosphate dikinase genedwere down-regulated, but starchconsuming enzymes such as heat shock proteins (HSP) and a-amylases were up-regulated, providing evidence for inhibited starch accumulation during grain development (Yamakawa et al., 2007). High temperature at ripening period of rice results in damaged (central chalky) grain which are round-shaped, loosely packed, and contain abnormal starch granules (Mitsui et al., 2013). Milky phase of rice grain development showed the prevalent impact of high temperature on the chalkiness of grains, which increases with increasing temperature (Tashiro and Wardlaw, 1991). Heat stress during grain development influences starch composition. For instance, amylose contents declined with heat stress which altered the fine amylopectin structure, which is the indicative of irregular starch synthase expression, and is an essential element responsible for the chalkiness of grains in rice (Inouchi et al., 2000). In rice, the amylose content in starch is a key factor when evaluating grain quality. Heat stress during grain development enhances the accumulation of dry matter in grain, but reduces the period of grain filling. In rice, with each 1
C rise in ambient temperature (25
C), period of grain development decreases up to three days, which reduces average weight of grains and fraction of mature grain (Tashiro and Wardlaw, 1991). High temperature at 35/30
C for the period of grain filling abridged the expression of elongation factor 1b and allergens, but increased the expression of glyceraldehyde-3-phosphate dehydrogenase (GAPDH), small heat shock proteins (sHSP) and prolamin, when compared with control temperatures (30/25
C) (Lin et al., 2005). Several cultivars responded differently to heat stress, including high chalky types, and sHSP were positively associated with the chalky-type kernel appearance (Lin et al., 2005). Under heat stress, the build up of all kinds of storage proteins boosted during primary maturing stage, while accumulation of prolamin decreased at maturity (Lin et al., 2010). In rice, chalky grain contained less prolamin, indicating an association between chalky structure and prolamins in grain, and that heat stress affects storage protein expression during grain filling (Lin et al., 2010). High night-time temperatures reduced the accumulation of pyruvate phosphate dikinase (PPDK) and pullulanase (PUL) isoforms; in this regard, PPDK was up-regulated and PUL was down-regulated during grain filling (Li et al., 2011). 3.2.2. Rate and duration of grain filling Heat stress during grain development increases the rate and diminishes the grain filling duration, leading to low grain weight and grain yield. Heat stress reduces the time of assimilate translocation during grain filling (Farooq et al., 2011). Under heat stress, earlier cessation of grain filling in temperate rice cultivars was not due to the lack of assimilates, but to the premature senescence of leaves (Kim et al., 2011). High temperature at flowering and grain filling, decreases grain yield due to spikelet sterility and a shorter grain-filling period. High night-time temperature of 22/34
C highly suppressed the grain weight, as compared with high daytime temperature of 34/22
C and the control (22/22
C) (Morita et al., 2005).

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3.2.3. Carbohydrate supply and grain growth Heat stress reduces the assimilate translocation to spikelets (Cao et al., 2008). When heat stress occurred after four days of heading, many aborted and opaque grains were observed (Tashiro and Wardlaw, 1991). In rice, heat stress during grain filling shows typical symptoms such as an enhanced rate of grain filling, low amylose contents, increased degree of chalkiness and reduced milling quality (Zhang et al., 2014a). Many enzymes linked to starch synthesis are regulated by heat stress including enzymes such as SSS, GBSS and starch-debranching enzyme (DBE). Heat stress down-regulated the isoforms of enzymes like SBE isoforms (SBEI, SBEIIb and SBEIII), and up-regulated SSS isoforms (SSSIIb, SSSIIc, SSSIIIb and SSSIVa) and certain starch-consuming enzymes such as a-amylase (Amy1A, Amy3D and Amy3E), which explains the amylose low concentration in grains of rice (Hakata et al., 2012). In previous studies, heat stress down-regulated the expression of BEIIb and a cytosolic pyruvate orthophosphate dikinase (cyPPDKB), which increased the chalkiness of rice grain; it was proposed that cyPPDKB and BEIIb are two candidate genes with a critical role in the chalkiness of grain (Li et al., 2011). 3.2.4. Hormonal imbalances during grain filling and maturation Heat stress reduces spikelet fertility and changes the hormonal balance in florets. Heat stress alters the hormonal homeostasis, content, stability, compartmentalization and biosynthesis (Cao et al., 2008). In general, developing grain have higher CTKs level. Cell division is believed to be controlled by CTKs during grain development. Moreover, grain development rate is positively associated with indole-3-acetic acid (IAA) content in rice grains. In summary, high temperature at grain filling deteriorated the starch synthesis in rice grain, leading to less starch accumulation during ripening. Heat stress at ripening results in chalky grain with abnormal and round-shaped starch granules. All classes of storage proteins accumulate more during early ripening, and chalky grain reduces prolamins, indicating a relationship between chalky structure and prolamins in grain, and that heat stress affects storage protein expression during grain development. The response to heat stress with regard to expression of proteins is byzantine, and molecular level basis of chalkiness in grains remained unclear yet. Heat stress reduces final weight of grains significantly, being the product of the rate as well as period of grain development. Heat stress initially enhances grain growth during ripening, but it reduces grain development phase which consequently decreases grain weight and yield. 4. Strategies to improve tolerance against thermal stress The selection and improvement of crop varieties usually tend

towards yield enhancement under prevailing climatic conditions. In this section, the strategies to improve cold and heat tolerance in rice through selection and breeding (Table 3), genetic engineering, molecular tools (Table 4), and agronomic and other management practices are discussed. 4.1. Cold stress 4.1.1. Selection and breeding There are two main genera of cultivated rice, one is indica and the other one is japonica. There is more cold tolerance in japonica as compared with indica genotypes during reproductive developments (Mackill and Lei, 1997). The selection of cold-tolerant genotypes is required to transfer cold tolerance from various sources to cultivars which are locally adapted (Table 3). In Australia, development of a cold-tolerant genotype at 1
C below the existing lowest threshold levels would potentially improve productivity by $79 per ha per year, and varieties with 2
C and 3
C lower than the existing lowest threshold levels could have productivity gains of $121 and $142 per ha per year, respectively (Singh et al., 2005). In several breeding programs, cold water under field conditions has been used to assess different rice populations for cold tolerance. In Japan, for instance, the cold-tolerant genes have been introduced into different temperate japonica breeding lines successfully, selected from javanica genotypes such as Padi Labou Alumbis, Lambayque 1 and Silewah, under field environments (Saito et al., 2001). 4.1.2. Marker-assisted selection Marker-assisted selection remains an operational technique used for breeding cold-tolerant cultivars due to the progressive increase in the advancement of linkage maps and molecular markers. Different cold-tolerant quantitative trait loci (QTLs) have been recognized over the last 20 years; some of which have been discussed in this review (Table 4). In rice, QTLs linked with cold stress tolerance were recognized using restriction fragment length polymorphisms (RFLPs) (Takeuchi et al., 2001) and microsatellite/ simple sequence repeats (SSR) molecular markers (Suh et al., 2010). The SSRs are more suitable for efficient mapping and markerassisted selection due to their procedural efficacy as well as multifarious ability. The SSR markers are multi-allelic and codominant which can be effectively used in the germplasm of japonica and indica rice. Many methodologies, such as grouped PCR-based selection, near-isogenic line development, hunting for successes in expressed sequence tag (EST) databanks (Saito et al., 2004), fine mapping based on microsatellite markers such as recognized markers through widely adapted genetic orders, and map-based

Table 3 Mass screening methods and traits for tolerance against thermal stress during reproductive phases in rice. Stress type Cold stress

Trait Fertility (%) Fertility (%) Spikelet fertility

Heat stress

Spikelet fertility Spikelet sterility Spikelet fertility Spikelet fertility Spikelet fertility Spikelet fertility

Screening method


12 C for 3e5 days during young microspore stage Cool water (20 cm depth) at 19.4
C from the primordial stage to heading completion Maximum and minimum temperatures around panicle initiation, 28.7
C and 10.9
C for short duration genotypes and 24.4
C and 11.0
C for long-duration genotypes 17
C for 10 days during booting 33.7
C for <1 h 26, 34 and 38
C during anthesis, and 38
C beginning at least 1 h after flowering for 4 h 37.5
C during flowering using controlled temperature chambers 39
C during booting 38
C during flowering

References Koike et al., 1990 Kuroki et al., 2007 Nahar et al., 2009

Suh et al., 2010 Jagadish et al., 2007 Ishimaru et al., 2010 Kobayashi et al., 2011 Tenorio et al., 2013 Tenorio et al., 2013

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Table 4 QTLs associated with tolerance against thermal stress during the reproductive phase in rice. Stress type

Evaluated trait

Cross

Chromosomal location (QTL name)

Cold tolerance variation explained (%)

References

Cold stress

Spikelet fertility Spikelet fertility Spikelet fertility Spikelet fertility/ undeveloped spikelet Heading date (day)

japonica 02428  indica 3037 japonica 02428  indica 3037 japonica 02428  indica 3037 e

1 (Ste1) 1 (Ste2) 12 (Ste3) 4 (Ctb1, Ctb2)

32.1 19.4 16.9 e

Li et al., 1997 Li et al., 1997 Li et al., 1997 Saito et al., 2001

Cold-tolerant japonica Koshihikari  Cold-sensitive japonica Akihikari Cold-tolerant japonica Koshihikari  Cold-sensitive japonica Akihikari Cold-tolerant japonica Koshihikari  Cold-sensitive japonica Akihikari Cold-tolerant japonica Koshihikari  Cold-sensitive japonica Akihikari japonica M-202  indica IR50 japonica M-202  indica IR50 cold-tolerant tropical japonica Silewah  temperate japonica Hokkai241 Cold-tolerant Norin-PL8  Coldsensitive Kirara397 Cold-tolerant Lijiangheigu  Coldsensitive Reiziq japonica TR22183  indica Dasanbyeo japonica TR22183  indica Dasanbyeo japonica TR22183  indica Dasanbyeo Cold-tolerant ZL1929-4  Coldsensitive japonica Towada Cold-tolerant Hokkai-PL9  Coldsensitive Hokkai287 Cold-tolerant Ukei 840  Hitomebore Japonica Nipponbare  indica Kasalath Japonica Nipponbare  indica Kasalath Japonica Nipponbare  indica Kasalath Sensitive cultivar 4628  tolerant cultivar 996 Sensitive cultivar 4628  tolerant cultivar 996 IR64 (sensitive female parent)  N22 (tolerant male parent) IR64 (sensitive female parent)  N22 (tolerant male parent) and IR64 (sensitive)  Milyang23 (moderately sensitive)  Giza178 (tolerant) IR64 (sensitive)  Giza178 (tolerant) IR64 (sensitive)  Giza178 (tolerant) IR64 (sensitive)  Giza178 (tolerant) IR64 (sensitive)  Giza178 (tolerant) Milyang23 (moderately sensitive)  Giza178 (tolerant) Milyang23 (moderately sensitive)  Giza178 (tolerant) Milyang23 (moderately sensitive)  Giza178 (tolerant)

3 (qHD-3-2)

15.5

Takeuchi et al., 2001

6 (qHD-6)

50.5

Takeuchi et al., 2001

1 (qCL-1)

31.1

Takeuchi et al., 2001

7 (qCT-7)

22.1

Takeuchi et al., 2001

2 (qCTB2a) 3 (qCTB3) 4 (Ctb1)

16.8 16.5 e

Andaya and Mackill, 2003 Andaya and Mackill, 2003 Saito et al., 2004

4 (Ctb-1)

e

Saito et al., 2010

10 (qLTSPKST10.1)

20.5

Ye et al., 2010

2 (QTL 2.1)

16.7

Jiang et al., 2011

8 (QTL 8.1)

24.8

Jiang et al., 2011

10 (QTL 10.1)

22.9

Jiang et al., 2011

7 (qCTB7)

21.0

Zhou et al., 2010

8 (qCTB8)

26.6

Kuroki et al., 2007

3 (qLTB3)

24.4

Shirasawa et al., 2012

1 (qHT1)

8.9

Zhu et al., 2005

4 (qHT4)

17.3

Zhu et al., 2005

7 (qHT7)

13.5

Zhu et al., 2005

4 (qPF4))

15.1

Xiao et al., 2011

6 (qPF6)

9.31

Xiao et al., 2011

1 (qHTSF1.1)

12.6

Ye et al., 2012

4 (qHTSF4.1)

17.6

Ye et al., 2012, 2015

1 (qHTSF1.2)

15e22

Ye et al., 2015

2 (qHTSF2.1)

15e22

Ye et al., 2015

3 (qHTSF3.1)

15e22

Ye et al., 2015

4 (qHTSF4.1)

15e22

Ye et al., 2015

6 (qHTSF6.1)

20.6

Ye et al., 2015

11 (qHTSF11.2)

15.2

Ye et al., 2015

1 (qHTSF1.2)

15e22

Ye et al., 2015

2 (qHTSF2.1)

15e22

Ye et al., 2015

Heading date (day)

Culm length (cm)

Spikelet fertility

Spikelet fertility Spikelet fertility Spikelet fertility

Spikelet fertility/ undeveloped spikelet Spikelet fertility Spikelet fertility Spikelet fertility Spikelet fertility 13 traits related to cold tolerance Seed fertility Seed fertility Heat stress

Grain filling Grain filling Grain filling Pollen fertility Pollen fertility Spikelet fertility

Spikelet fertility

Spikelet fertility Spikelet fertility Spikelet fertility Spikelet fertility Spikelet fertility Spikelet fertility Spikelet fertility Spikelet fertility

(continued on next page)

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M.S. Arshad et al. / Plant Physiology and Biochemistry 115 (2017) 57e72

Table 4 (continued ) Stress type

Evaluated trait

Spikelet fertility

Spikelet fertility

Cross Milyang23 (moderately sensitive)  Giza178 (tolerant) IR64 (sensitive)  Milyang23 (moderately sensitive)  Giza178 (tolerant) IR64 (sensitive)  Milyang23 (moderately sensitive)  Giza178 (tolerant)

Chromosomal location (QTL name)

Cold tolerance variation explained (%)

References

6 (qHTSF6.1)

20.6

Ye et al., 2015

11 (qHTSF11.2)

15.2

Ye et al., 2015

cloning methods have remained used for genes identification, which are in charge of QTLs associated with tolerance to chilling stress during panical initiation phase in rice (Saito et al., 2004). Saito et al. (2001) identified two QTLs (Ctb-1 and Ctb-2) on chromosome 4 which were closely allied to chilling stress tolerance in rice, as well as proposed a relationship with anther length (Table 4). Subsequently, Saito et al. (2004) described the physical mapping and putative candidate gene identification of a QTL (Ctb1) destined for the tolerance of cold stress at panicle initiation phase and proven the anther length relationship with Ctb1 in rice (Table 4). In recent years, Saito et al. (2010) identified F-box protein gene and linked the long anther length with tolerance to cold stress. These authors reported that the F-box protein acts with Skp1 (S-phase kinase-associated protein 1), a subunit of E3 ubiquitin ligase, and suggested that the ubiquitin-proteasome pathway is associated with tolerance to cold stress during panicle initiation (Saito et al., 2010). Anther length directly influence the fertilization as the pollen availability is necessary for successful fertilization, and maturity of pollen is also affected by cold stress which reduces fertility. Cold-tolerant varieties have long anthers and, thus, they produce more pollen than sensitive varieties. Thus, a strong relationship was proposed amongst the QTLs linked with anther length and cold stress tolerance, showing that the number of pollen grains was a significant factor for the mechanism of tolerance (Saito et al., 2001). In rice, Takeuchi et al. (2001) built a connection using RFLP and random amplified polymorphic DNA (RAPD) molecular markers along with the identification of eight QTLs responsible for tolerance to cold. From those eight, the authors identified QTLs which contributed more commonly for tolerance under cold (qCT-7 on chromosome 7), and the tolerance of cold stress associated with heading date (qHD-3-2 on chromosome 3 and qHD-6 on chromosome 6) and culm length (qCL-1 on chromosome 1) which explained 22.1%, 15.5%, 50.5% and 31.1% of phenotype variance, respectively (Table 4). Using SSR markers to analyze the F2, F3, and F7 generations, a cold tolerant QTL during booting in rice was also identified on chromosome 8 (qCTB8) which explained 26.6% of phenotype variation (Table 4; Kuroki et al., 2007). Approximately 30 open reading frames (ORF) have been identified in the qCTB8 region, one which encodes monodehydroascorbate reductase (MDAR) and exhibited up-regulation with the cold treatment of rice anthers during the stage of young microspore (Kuroki et al., 2007). Another cold tolerance related QTL during booting phase has been described on chromosome 7 (qCTB7), which elucidated 9% and 21% of phenotype variation in F2 and F3 populations, in respective order. By means of mapping and cloning, 12 putative cold-tolerant genes were identified from this QTL region (Table 4; Zhou et al., 2010). Using physical and genetic mapping, previously identified qCT7 (Takeuchi et al., 2001), may be present at the same locus as qCTB7. Despite being recognized from different genetic environments and backgrounds, these three QTLs described

comparable fractions for phenotypic variation, fluctuating between 20.6% and 22.1% (Zhou et al., 2010). Chromosome 3 at its long arm contained a single QTL (qLTB3), tolerant to cold stress during booting, which elucidated 24.4% of phenotype variation (Table 4; Shirasawa et al., 2012). From five genes present in the region of qLTB3, seven single nucleotide polymorphic (SNP) markers were recognized, all of which act as amino acid substitutes. Among those, one present in the Os03g0790700 gene results in a mutation in a preserved amino acid and is thought to be a strong candidate for cold tolerance (Shirasawa et al., 2012).

4.1.3. Genetic engineering Genetic engineering is alteration of an organism's hereditary makeup through artificial methods, every so often comprising on a specific genes transfer from one species to another. Chen et al. (2002) sequenced the full genome of rice, permitting the identification and localization of genes associated with stress tolerance. To identify homologs of other species, the rice system may be used to allocate gene functions. To recognize general plant processes, the association between genomes may help in the efficient use of genomic methodologies for rice plants, particularly in response to thermal stress. Genetic engineering permits the insertion of a single gene into candidate genotypes as well as compromises many chances for the enhancement of tolerance to ecological stresses (Koh et al., 2007). Numerous genes in rice which are responsive to chilling stress have been isolated and characterized. Many cold-tolerant genes, particularly those from the CBF/DREB1 (C-repeat binding factor/dehydration responsive element binding) family, act as enzymes and seem to be linked with tolerance under cold with encoded proteins for the biosynthesis of osmoprotectants, chaperones, and signaling mechanisms (Xie et al., 2012). The method of the selection of T-DNA labeled plants of rice under cold, is being utilized to recognize the responsive genes for cold stress. By using the T-DNA tagged technique along with inverse PCR, researchers can isolate and characterize genes at the molecular level, including OsGSK1 (glycogen synthase kinase3-like 1), OsRLK1 (a putative leucine-rich repeattype receptor-like protein kinase) and OsDMKT1 (a putative demethylmenaquinone methyltransferase) (Koh et al., 2007). The gene OsGSK1, an orthologue of Arabidopsis brassinosteroid insensitive 2 (BIN2), enhanced the tolerance in rice for cold stress, by acting as a down-regulator of brassinosteroid (BR) signaling, when knocked out (Koh et al., 2007). Transgenic production may be an attractive option for improving cold tolerance in rice, by disrupting or introducing a particular DNA sequence. The effective genetic transferal procedures and advancements within recombinant DNA technology have led to the effective transformation and production of transgenic lines.

M.S. Arshad et al. / Plant Physiology and Biochemistry 115 (2017) 57e72

4.2. Heat stress 4.2.1. Selection and breeding In rice, it is suggested that pollen fertility provides an index for selection and breeding under heat stress (Cao et al., 2009). In China, heat-tolerant hybrids of rice such as Guodao 6 and Xieyou 46 have been developed with a stable high rate of grain setting and spikelet fertility under heat stress; the grain-setting stability of Guodao 6 is due to its heat avoidance adaptability by erratic floral traits, such as shortened flowering phase and weakened “apical grain superiority” (Tao et al., 2008). Most tolerant cultivar, Fusaotome has been used for breeding purpose, along with some moderately tolerant cultivars such as Hanahikari, Koshijiwase and Tentakaku (Ishizaki, 2006). In rice, several important traits used for breeding are quantitatively inherited. A good knowledge of the genomic bases with DNA markers may be advantageous in setting up a suitable breeding plan for multigenic traits (Krishnan et al., 2011). 4.2.2. Marker-assisted selection Heat stress responses are controlled by multiple genes; hence, information on the nature of QTLs used for tolerance to heat stress is limited (Zhu et al., 2005). However, different QTL studies related to heat tolerance using molecular markers have been acknowledged. Zhu et al. (2005) identified three QTLsdusing a backcross inbred line (BIL) population from a japonica/indica cross of Nipponbare/Kasalathdfor heat tolerance during grain development on chromosome numbers 7, 4 and 1, which elucidated 13.5%, 17.3% and 8.9% of phenotype variance, in respective order (Table 4). Of these, a QTL present on chromosome 4 in the C1100-R1783 region exhibited no epistatic effects or association between the QTL and the environment. At flowering stage, some other QTLs related to tolerance under heat stress, have been documented, which were isolated from recombinant inbred lines produced from crosses of indica/ indica and indica/japonica (Zhang et al., 2008). In China, QTLs linked to heat stress tolerance were identified from recombinant inbred lines developed by crossing a sensitive cultivar 4628 with a heat-tolerant rice cultivar 996. In field experiments, rice genotypes were exposed to heat stress during flowering phase, and tolerance to heat stress was evaluated using fertility of pollen as an indicator. Using composite interval mapping (CIM) examination, two QTLs (qPF4 and qPF6) affecting pollen fertility were identified between RM471 and RM5687 on chromosome 4 and between RM225 and RM190 on chromosome 6. These QTLs, qPF4 and qPF6, described 15.1% and 9.31%, respectively, of entire pollen fertility phenotype variance in rice subjected to heat stress, and enhanced pollen fertility by 7.15% and 5.25%, respectively (Table 4; Xiao et al., 2011). The qPF4 QTL, present in the highlytolerant cultivar 996, may prove beneficial for the development of new genotypes of rice having enhanced tolerance against heat stress. Among various QTLs in rice, qHTSF4.1 was a better source at flowering for high temperature tolerance (Table 4; Ye et al., 2015). Many other QTLs have been reported (Table 4). Major QTLs that have been identified could be useful for further gene cloning and fine mapping, as well as marker-assisted molecular breeding for high temperature tolerant rice genotypes. Mapping studies may be advantageous for isolating genetic regions related to most inherited traits; under certain situations, it may be possible to identify the specific gene for a QTL (Krishnan et al., 2011). 4.2.3. Genetic engineering Genetic engineering tools have been successfully employed to induce heat tolerance in several plant species, mainly through the overexpression of HSP genes otherwise indirectly through changing the transcription factors level of HSP. High concentrations of osmolytes also induced tolerance against heat stress through

69

varying membrane fluidity as well as cell detoxification enzymes (Farooq et al., 2011). Rerksiri et al. (2013) identified six genes (Os05g0381400, Os03g0745000, Os09g0526600, Os11g0453900, Os04g0107900 and Os06g0195800) by microarray analysis that rice panicles produced under heat stress and were highly responsive to heat stress; using quantitative real-time PCR (qRT-PCR), and the expression pattern of these six genes was fixed in different organs under abiotic stresses. Three promoters of highly heat-responsive genes (PM19p, Hsp90p and OsHsfB2cp) were used to drive the expression of the GUS (b-glucuronidase) gene in rice. GUS gene expression was confirmed by GUS activities and histochemical staining in the flag leaves and panicles of transgenic rice under heat and drought conditions. All three promoters showed equally high activity levels in rice leaves; in this regard, PM19p and OsHsfB2cp exhibited high activities in the panicles under heat stress conditions. Rerksiri et al. (2013) confirmed that PM19p and OsHsfB2cp were highly heat responsive; further reconstruction and characterization of cis-elements in their respective promoters may lead to the development of more effective heat-responsive promoters for the genetic engineering of rice plants. Basmati rice was engineered for heat tolerance by overexpression of the hsp101 gene. Different lines of transgenic rice exhibited further growth during the recovery period after heat stress, whereas untransformed plants never recovered to the same extent (Katiyar-Agarwal et al., 2003). In summary, genetic variation is necessary to prevent inbreeding; fortunately, the rice species has a broad range of adaptation to thermal stresses, and tolerant ecotypes are also available for breeding purposes. Adaptation and breeding to cold stress were by far more successful than breeding for heat stress in rice, however a suitable selection method is essential for assessing thermal stress tolerance in segregating populations using controlled air or water temperatures. Breeding practices have been effective in the development of thermal tolerance during the reproductive development of rice; both avoidance as well as tolerance are suitable traits to initiate breeding programs for rice grown in warm climates. 5. Management strategies Crop management strategies can improve resistance against cold and heat stress in rice. The most effective and commonly-used practice in tropical low-altitude systems, is to increase the deepness of water up till panicle initiation in rice, to minimize losses due to low temperature. Deep water significantly shields the rice crop from injury during the start of pollen microspore phase which is highly cold-sensitive, as the temperature of deep water (20e25 cm depth) remains generally 6
Ce7
C more as compared to nighttime temperatures (Singh et al., 2005), this depends extremely on the system and its location. Balanced crop nutrition is another strategy to prevent rice from succumbing to temperature stress. However, during unpredictable weather conditions, one strategy to defend rice from cold injury is to apply a less-than-optimal amount of nitrogen. While this approach may protect the crop from cold stress, as the plants are small and probably protected by the water, the low nitrogen levels may result in low grain yields. In this regard, novel rice varieties which may tolerant to cold stress, can help the farmers for the enhancement of nitrogen use up to its optimal, it will increase the production at least up to 5% (Singh et al., 2005). Shifting the planting time is another management strategy in some regions. Early planting may avoid damage from cold stress, and late planting may escape heat stress (Singh et al., 2005). While high temperatures can occur during grain development, late planting may escape terminal heat stress allowing grain to develop

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in the cooler environment. Crop duration was more influenced by the sensitivity of rice genotypes to temperature and photoperiod, as the rice genotypes are short-day in nature. Crop period was affected in the same way by sowing date, genotypic selection, and year, in high altitude, however in mid altitudes, cultivars not showed any influence, and at low altitudes sowing date was highly affected (Shrestha et al., 2013). Cold stress at high altitudes adversely affected the grain yield, and at low altitudes, it was highly influenced by frequent tropical cyclones (Shrestha et al., 2013). Duration of a crop primarily be determined by genetic period of primary phase of vegetative development, at temperature range 20e30
C, and photoperiod of <12 h (Shrestha et al., 2013). Under inductive conditions, after a few days of the basic vegetative phase, it shifted to panicle initiation. The rice genotypes, which showed insensitivity to photoperiod, have the smallest photoperiod sensitive period (Shrestha et al., 2013). Japonica genotypes are less responsive to photoperiod than temperature as compared to indica cultivars. In summary, any of the management practices described above may be successful in the prevailing environmental conditions of a region. However, the development of varieties in collaboration with plant breeders, biologists and agronomists may overcome these problems more efficiently. 6. Conclusion and future research thrusts Substantial grain yield losses occur in rice due to thermal stress. Cold stress impedes various growth and reproductive processes in rice. It delays panicle initiation and thus flowering, and affects anther respiration which can enhance sucrose accumulation, protein denaturation and asparagine levels, and reduce proline accumulation. The entire developmental process starting from gamete formation to fertilization and grain development is sensitive under cold stress. Cold stress causes pollen sterility due to tapetal hypertrophy and the related nutrient imbalances. Cold stress may impair pollination due to inhibited anther dehiscence, stigma receptivity and the ability of the pollen tube to germinate to the style. Cold stress causes floret sterility which reduces the final grain yield. It also reduces the rate as well as period for grain filling, which may increase abortion rate and reduce seed size. Various studies on temperature-stress responsive genes have shown that some molecular and physiological modifications occur with cold acclimatization, and many metabolic processes are affected by cold stress which indicates that cold tolerance is complicated. As a result, cold stress brings severe economic and social shocks because the reproductive phase directly impacts economic yield and food security. Heat stress in rice causes anther indehiscence by restricting locule closure which leads to reduced pollen dispersal. Heat stress modifies pollen proteins, which may significantly reduce pollen viability and pollen tube length, with poor anther dehiscence and fewer pollen on the stigma. Thus, heat stress causes spikelet sterility. Heat stress delays flowering and affects pre-fertilization more than post-fertilization development. Starch synthesis diminishes under heat stress during grain development stage in rice, which results in less starch accumulation at the ripening stage. Heat stress results in chalky grain at the ripening stage in rice, which have irregular and round-shaped starch granules. Heat stress may increase the rate of grain filling, on the other hand it shortens the period of grain filling, which causes substantial yield losses. Breeding practices are effective in case of rice, for inducing heat stress tolerance during reproductive stage; both avoidance as well as tolerance, are useful characters for rice breeding programs in warm weather conditions. Several heat-stress responsive rice genes have been identified and characterized and need further attention

from plant breeders and researchers. Despite progress with thermal stress tolerance in rice, cold and heat stress still reduce yield, particularly where indica rice is grown. Genetic variation is required in breeding. Fortunately, the rice species has widespread adaptation to cold stress and cold-tolerant ecotypes exist for breeding material. A comprehensive approach is needed to recognize the basic mechanisms for cold tolerance, despite to ascertain several genes of cold tolerance. Use of gene pyramiding and gene promoters should be encouraged. Modern techniques, such as large-scale sequencing, microarray analysis and proteomics, should explain more in the future. Heat stress negatively affects mitosis in rice; its role to induce pollen abortion at mitosis through its effects on the tapetum is not clear and needs to be investigated. The response to heat stress is complicated with regard to the expression of storage proteins, and the molecular mechanism of grain chalkiness. Research on the mechanisms of assimilate translocation to spikelets to avoid poorly filled grains, and phenotypic plasticity is needed. For better rice production on a sustainable basis, the response and tolerance mechanisms need to be explored at the molecular level, e.g. QTL studies. A functional genomics approach can be used for the understanding of molecular basis regarding rice response to heat stress tolerance. For future research, an important field of study is the isolation of allelic sources for heat stress tolerance, and their integration into advanced lines using conventional breeding techniques, and modern molecular and biotechnological tools. Modern genomics and ecophysiological investigations may help to understand the interaction between genotypes and temperature stress. New rice varieties for cold and heat tolerance at the reproductive stage are needed to overcome yield losses. Contribution MSA and MF conceived the idea and outline the review manuscript. MSA prepared the first draft. MF, FA, JSVK, PVVP and KHMS finalized the manuscript. References ADB., (Asian Development Bank), 2009. The Economics of Climate Change in Southeast Asia: a Regional Review. Manila, the Philippines. Ahmed, N., Maekawa, M., Tetlow, I.J., 2008. Effect of low temperature on grain filling, amylose content and activity of starch biosynthesis enzymes in endosperm of basmati rice. Aust. J. Agric. Res. 59, 599e604. Andaya, V.C., Mackill, D.J., 2003. QTLs conferring cold tolerance at the booting stage of rice using recombinant inbred lines from a japonica 9 indica cross. Theor. Appl. Genet. 106, 1084e1090. Cao, Y.Y., Duan, H., Yang, L.N., Wang, Z.Q., Liu, L.J., Yang, J.C., 2009. Effect of high temperature during heading and early filling on grain yield and physiological characteristics in Indica rice. Acta. Agron. Sin. 35, 512e521. Cao, Y.Y., Duan, H., Yang, L.N., Wang, Z.Q., Zhuo, S.C., Yang, J.C., 2008. Effective heat stress during meiosis on grain yield of rice cultivars differing in heat tolerance and its physiological mechanism. Acta. Agron. Sin. 34, 2134e2142. Chen, M., Presting, G., Barbazuk, W.B., Goicoechea, J.L., Blackmon, B., et al., 2002. An integrated physical and genetic map of the rice genome. Plant Cell 14, 537e545. Das, S., Krishnan, P., Nayak, M., Ramakrishnan, B., 2014. High temperature stress effects on pollens of rice (Oryza sativa L.) genotypes. Environ. Exp. Bot. 101, 36e46. Dingkuhn, M., Radanielinac, T., Raboina, L.M., Dusserrea, J., Ramantsoanirinad, A.,
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