Physiology of Spikelet Development on the Rice Panicle

C H A P T E R

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Physiology of Spikelet Development on the Rice Panicle: Is Manipulation of Apical Dominance Crucial for Grain Yield Improvement? Pravat K. Mohapatra,* Rashmi Panigrahi,* and Neil C. Turner† Contents 1. Introduction 2. Panicle Structure and Development 2.1. The morphology of spikelets 2.2. Ontogeny 2.3. Heterogeneous development of spikelets 3. Panicle Architecture and Grain Yield 3.1. Heterogeneous architecture of the panicle and its relationship to grain yield 3.2. Modification of panicle morphology for improved grain filling 4. Physiological Factors Regulating Spikelet Development 4.1. Metabolic control of assimilate partitioning 4.2. Starch biosynthesis 4.3. Expression profile of the genes regulating the activity of starch biosynthesis enzymes 4.4. Hormonal regulation of spikelet development 5. Is Manipulation of Apical Dominance Crucial for Grain Yield Improvement? 6. Suggestions for Modification of Apical Dominance Acknowledgments References

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Abstract Cultivated rice, Oryza sativa L., originated in the flood plains of Asia with their variable environmental conditions. Heterogeneous architecture, leading to intergrain apical dominance in spikelet development, was an important strategy * School of Life Science, Sambalpur University, Sambalpur, India Centre for Legumes in Mediterranean Agriculture and UWA Institute of Agriculture, The University of Western Australia, Crawley, WA, Australia

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Advances in Agronomy, Volume 110 ISSN 0065-2113, DOI: 10.1016/B978-0-12-385531-2.00005-0

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2011 Elsevier Inc. All rights reserved.

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for plant survival under such uncertain conditions. When inclement weather conditions coincide with the sensitive stage of spikelet development, the plant sacrifices some spikelets while preserving the rest to enable some grains to fill to provide seed for the next generation. The nature of the interaction between a genotype and its environment determines the ultimate spikelet number. This heterogeneous architecture was considered a liability for the increased demand for food. Innovative breeding efforts have changed the plant type in favor of extra-heavy panicles bearing a large number of spikelets, mostly in a homogeneous distribution. However, the reduced intergrain apical dominance decreased the strength of the sink for assimilate partitioning to the spikelets, much to the detriment of increased grain production. The metabolic control of assimilate partitioning and the genes controlling starch synthesis are reviewed and the importance of hormonal control of grain filling is emphasized. A model has been constructed to project the role of metabolites, hormones, and other factors in intergrain apical dominance. The panicle architecture of rice is amenable to modification by both intrinsic and extrinsic factors, and there is extensive variation of panicle structure among genotypes. Therefore, we suggest that an architecture with controlled intergrain apical dominance, amounting to production of a greater number of responsive sinks, which is a compromise between heterogeneous and homogeneous architecture of the inflorescence, should benefit spikelet filling in rice with large panicles.

1. Introduction Rice is the staple food for half of the human race. Most rice consumers live in the tropics and subtropics of Asia, where in many cases, the irrigation infrastructure cannot support the year-round cultivation of any major cereal. While heavy monsoonal rains, usually confined to only 2–3 months of the year, allow rice cultivation in the region, cropping is limited to rice because the soils become too waterlogged for other crops. Man and domestic animals thrive on the success of rice cultivation, unless the monsoon is fickle and the crop suffers from high abiotic stress. According to Virk et al. (2004), global rice yield, which is 645 million tonnes today (FAOSTAT, 2010), must reach 800 million tonnes in 2025 to meet the demand for rice consumption. This extra rice will have to come from improvements in irrigated rice because the environmental stresses of rainfed rice are hard to overcome (Cassman, 1999). Currently, irrigated rice occupies just over 57% of the 150 million ha of land under rice production (International Rice Research Institute, 2010), but contributes 76% of the global production. To meet the challenge and boost production, the United Nations declared rice as the crop of the year in 2004; major attention was given to improving the production of irrigated rice. The average yield of irrigated rice will have to increase from 4 to 8.5 tonnes ha
1 to meet this challenge (Peng et al., 1999).

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Based on the total amount of incident solar radiation, Yoshida (1981) estimated that the theoretical yield potential of rice is 15.9 tonnes ha
1, but the vagaries of climate scale the yield potential back to 8.5 tonnes ha
1 (Matthews et al., 1995). Ample scope exists for achieving this target, provided researchers successfully pyramid all the known beneficial traits in a new plant type (NPT).

2. Panicle Structure and Development 2.1. The morphology of spikelets The rice plant bears a panicle with determinate inflorescences on the terminal end of the shoot (De Datta, 1981). The panicle bears a central axis (rachis) which extends from the base (neck node) to the tip of the axis, indicated by a minor swelling at the base of the terminal primary branch (Fig. 1). The axis has 8–10 nodes at intervals of a few centimeters from which primary branches emerge (Fig. 1). Secondary branches develop on the primary branches in similar fashion (Fig. 1). Pedicels develop from the nodes of primary and secondary branches; each pedicel culminates with a spikelet at the terminal end (Yoshida, 1981). Unlike other cereals, spikelets are considered the individual floral units of the complex inflorescence of rice. Each spikelet bears one grain at maturity (Xu and Vergara, 1986). A spikelet consists of two sterile lemmas, the rachila, and the fertile floret (De Datta, 1981). The rachila is the small axis between the fertile floret and the sterile lemmas. The fertile floret bears a pistil with uniovulate ovary and feathery and bifid stigma. The androecium has six two-celled anthers borne on slender filaments. The androecium and gynoecium are enclosed in the space between two hardened bracts named lemma and palea; the former is five-nerved and bears an awn compared to the awnless three-nerved palea.

2.2. Ontogeny The initiation of panicle primordia occurs at the tip of the vegetative stem apex inside the boot of the flag leaf sheath 30 days before flowering. The dome of the vegetative apex elongates to mark the change to reproductive development. Neck node differentiation is the first step of panicle development and the event closes with maturation of pollen grains at the time of flowering. Initially, the young panicle remains shrouded with colorless hairs; it becomes visible after becoming about 1-mm long (Matsushima, 1970; Xu and Vergara, 1986; Yoshida, 1981). As the panicle axis extends upward and reaches a length of 50 mm, spikelet primordia are differentiated on the primary and secondary branches (De Datta, 1981) and the total number of

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Group I Group II Group III Group IV Group V Group VI Group VII

Spikelet

Secondary branch Primary branch

Panicle axis

Figure 1 Schematic of the rice panicle showing the panicle, primary branches, secondary branches, and the spikelets that flowered each day for 7 days (Group I on day 1 to Group VII on day 7). Groups I–III are considered superior spikelets and Groups IV–VII are considered inferior spikelets. From Mohapatra et al. (1993), with permission.

spikelets in the panicle is determined. The coincidence of inclement weather, resulting in any form of environmental stress at this crucial stage, limits spikelet number, and ultimately, the grain number and yield at maturity.

2.3. Heterogeneous development of spikelets During ontogeny, the spikelet primordia differentiate on the primary and secondary branches of the rice panicle (Xu and Vergara, 1986). Initiation of primary branches on the panicle axis, secondary branches on primary

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branches, and spikelets on both the branches occur in acropetal succession from the base to the top of the panicle (Fig. 1; Murata and Matsushima, 1975; Xu and Vergara, 1986). However, the development of these organs does not follow the same order. The upper branches and spikelets (Groups I–III in Fig. 1) emerge from the flag leaf sheath (boot) first and are the first released from the physical constraints of the flag leaf enclosure. Contact with light encourages faster development of these apical branches and spikelets, while the basal spikelets (Groups IV–VII in Fig. 1) and branches develop more slowly while they are still within the sheath of the flag leaf. Therefore, primary branch development is progressively delayed in the basipetal direction, while initiation is the opposite (Xu and Vergara, 1986). Lack of homogeneity in development has led to a wide variation in individual grain weight of the spikelets across the rice panicle. Frequently, many spikelets on the basal primary branches do not bear a mature grain. The poorly or partially filled basal grains are also of poor quality and low market value (Mohapatra et al., 1993; Venkateswarlu et al., 1986a,b).

3. Panicle Architecture and Grain Yield 3.1. Heterogeneous architecture of the panicle and its relationship to grain yield Variation in grain weight and quality within a panicle is dependent on panicle architecture. The number of poorly filled grains increases significantly when the panicle size is large because most of the grains on the spikelets on the secondary branches of the panicle become source-limited for assimilates (Kato, 2004). It is possible that poor translocation and partitioning of assimilates from the source leaves and stems at crucial stages of grain filling fails to sustain development of a large number of spikelets (Yang et al., 2002a). However, starch synthesis in the endosperm cells of the spikelets on secondary branches is poor (Umemoto et al., 1994) and assimilates partitioned to them remain unused so that the sink may be the impediment to the transport and storage of assimilates. Spikelets located on the upper primary branches that flower early exert dominance, accumulate larger amounts of starch, and produce better quality grains than lateflowering spikelets on secondary branches (Ishimaru et al., 2003; Mohapatra et al., 1993; Yang et al., 2006a). It has been speculated that in rice, improvement of panicle size due to increased sink strength would induce greater source activity and biomass production (Toenniessen, 1991). The nature of the source–sink relationship in dry matter partitioning to the panicle from source leaves has been worked out by partial removal of competing sink organs from the developing panicle in contrasting rice cultivars. Using the stable isotope of carbon, Mohapatra et al. (2004) reported that the growth

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and development of the spikelets of the high-yielding rice cultivar “Takanari” was sustained by photosynthates from the upper three leaves, whereas in the traditional rice cultivar “Nakateshinsenbon,” spikelet growth was supported by assimilates from the flag leaf only. Nevertheless, at present, the relationship between photosynthesis and grain filling is poorly understood. The so-called NPT of rice (Dingkuhn et al., 1991; Sheehy et al., 2001; Virk et al., 2004) and hybrid rice (Zhu et al., 1997) has been developed for increased biomass production with higher carbon assimilation capacity under conditions of high radiation and temperature in the tropics (Khush, 1996). In spite of this increased source activity, many spikelets remain unfilled or poorly filled in the extra-heavy panicles of these newly improved cultivars. Murchie et al. (2002) showed that there was no association between grain-filling rate and light-saturated photosynthesis in any of the five NPT lines and one indica rice studied, while Scoefield et al. (2002) reported that antisense suppression of the rice sucrose transporter gene that impaired grain filling did not affect photosynthesis.

3.2. Modification of panicle morphology for improved grain filling In cereals, the number of spikelets is one of the major components of grain yield (Feil, 1992). An increase in the size of the panicle by increasing spikelet number enhances spikelet number per unit area in the field as well as the yield potential of the crop (Peng et al., 1994). Because individual kernel weight and panicle number per plant in rice appear to be genetically fixed (Luo et al., 2001; Zhikang et al., 1997) and stable for decades (Evans et al., 1984), seed number per panicle is believed to be amenable to genetic modification. Plasticity in spikelet/seed number per panicle has been reported under a range of agroclimatic conditions in which rice is grown (Kropff et al., 1994). Using an empirical model of yield, Sheehy et al. (2001) predicted that the grain yield potential of rice would double if all of the juvenile spikelets were transformed into grains. An improved reproductive sink capacity along with an extended grain-filling period were two of the traits used in the rice breeding program to improve the semidwarf plant type and develop a new plant ideotype (Dingkuhn et al., 1991). Compared to indica types, the NPTs used tropical japonica germplasm to increase the size of the panicles (Peng et al., 1994). Similarly, intercrossing between japonica and indica rices resulted in hybrids bearing panicles larger than conventional inbred rice (Zhu et al., 1997). However, an increase in the number of spikelets does not always result in high grain number and a yield benefit at maturity because the degree of grain filling of individual spikelets depends on the position of the spikelet within a panicle (Kato, 2006). Spikelets located on distal parts and the primary branches of the panicle (Groups I–III in Fig. 1, hereafter called superior spikelets) possess

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grain-filling attributes that are better than those spikelets located on proximal parts and/or secondary branches (Groups IV–VII in Fig 1, hereafter called inferior spikelets; Ishimaru et al., 2003; Mohapatra et al., 1993). Kato (2006) used a panicle centroid index, which is a mathematical index to represent distribution of spikelets on various primary branches of the panicle axis, as a criterion for assessing grain-filling efficiency of four extra-heavy and two non-extra-heavy panicle types of rice cultivars by comparing proximally versus distally laid spikelets of the panicle. Cultivars possessing a higher panicle centroid index, that is more superior spikelets, also showed a higher proportion of high-density (specific gravity) grains in the panicle. However, the number of spikelets on secondary branches of the panicle exhibited a stronger relationship with grain filling than that of the panicle centroid index. The increase in the number of spikelets, on secondary branches was found to contribute to the increase in the total number of spikelets per panicle in extra-heavy panicle types. Padmaja Rao (1987) instead used the percentage of high-density grains on the lowermost primary branch of the panicle, which is the least favored destination for assimilates, as an index for screening the grain-filling potential of a cultivar. The panicle architecture of traditional rice is simple. Most of the spikelets are borne on the primary branches and the percentage of filled grains on the panicle is high, but the overall grain yield of the panicle is poor because of a low spikelet number. Breeding for increased spikelet number per panicle was successful in many cultivars, but the extra spikelets were mostly located on secondary branches of the panicle (Kudo, 1991; Yamamoto et al., 1991), and as these spikelets do not fill as efficiently as the spikelets on primary branches, the objective of achieving high-yield potential was not realized (Kato, 1993). A comparison of the percentage contribution of filled, half-filled, and empty spikelets to the total spikelets at various spatial locations of the panicle of indica inbred, indica hybrid, and the NPT rice cultivars confirmed this (Khush and Peng, 1996); the spikelet number in the NPT is higher than other types, but the number of filled grains did not increase (Yang and Zhang, 2010). Similarly, Yang et al. (2000) reported that the indica inbred cultivar IR72 exhibited a high rate of grain filling, whereas some of the NPT rices derived with tropical japonica background did not. The grain number per panicle in rice is a function of panicle length and grains per unit length of panicle (Sheehy et al., 2001). However, increasing the panicle size or height could have a detrimental effect on light interception and the rate of photosynthesis of the source leaves which are positioned beneath the panicle and supply assimilates to the grains during development (Setter et al., 1996; Xu et al., 1990). Therefore, breeders of the extra-heavy super rice have selected for more spikelets per unit length of panicle to increase spikelet number per panicle without any appreciable increase in panicle length. This increased compactness of the panicle allows large number spikelets to be accommodated on the panicle. However, the

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increased compactness reduces the grain quality of the spikelets on secondary branches as a result of increased variation in the length, width, length–width ratio, chalky grain percentage, and amylose content of the grains on the rice panicle (Wang et al., 2008). On the other hand, the spikelet development of rice with lax panicles is not impeded by space restrictions and the cultivars produce grains with larger biomass (Panda et al., 2009). Lack of freedom from either spatial confinement on the panicle axis (compact panicle) or temporal confinement inside the flag leaf sheath (late emergence of basal spikelets) affects spikelet development and results in the production of poor-quality grains.

4. Physiological Factors Regulating Spikelet Development Determination of seed number is an important component of grain yield in all grain crops. Therefore, it is important to understand the relationship between the number of spikelets when they differentiate, and the number of grains at maturity in the panicle of rice. The physiological significance of the processes of production of a large number of reproductive units (spikelets) on the flowering axis (panicle) during ontogeny and elimination of many of them prior to grain maturity, especially in the rice with heavy panicles, has not received enough attention by rice scientists. The survival of spikelets in a cultivar may be related to the degree of interaction between the biological and environmental factors that control partitioning of assimilates to the developing spikelets. Cultivated rice was domesticated on the undulating flood plains of Asia, resulting in both drought and floods (Oka, 1991). The production of an excess of reproductive structures that could be sacrificed depending on the seasonal conditions in the adaptation of rice to its environment may be responsible for the source–sink relations and assimilate partitioning of the present-day rice plant. Several authors have examined the source–sink relations of rice by assessing the metabolic and hormonal control mechanisms of spikelet development, as will be discussed in the next sections.

4.1. Metabolic control of assimilate partitioning Increased partitioning of assimilates into the reproductive organs has contributed significantly to the improvement of the yield potential of crops (Gifford and Evans, 1981). Similarly in rice, there has been a marked increase in harvest index and grain production by modification of the reproductive structures in the modern cultivars, but the source activities like photosynthetic rate and crop growth rate have remained unchanged for decades (Evans et al., 1984). Efforts undertaken to increase biomass production or

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the photosynthetic rate of rice have not contributed to any increase in yield potential (Vergara, 1987). Intensive study is necessary to improve the assimilate partitioning in favor of spikelets on the secondary branches and raise the number of high-density grains in the panicle in order to achieve a high yield potential (Padmaja Rao et al., 1985; Vergara, 1987; Vergara et al., 1990) and break the yield barrier of irrigated rice (Khush and Peng, 1996). Nishiyama (1983) observed wide variation in the cross-section of the phloem in the pedicel of spikelets positioned on different parts of the rice panicle. Spikelets bearing high-density grains possessed larger phloem (Nishiyama, 1983) and better developed vascular bundles (Chaudhry and Nagato, 1970). The situation was similar in the panicles of cultivars with extra-heavy panicles that had better developed vascular bundles and phloem. Such variation in vascular structures could lead to differences in assimilate supply between the developing spikelets, resulting in heterogeneous growth and formation of qualitatively different types of grains in the rice panicle (Padmaja Rao et al., 1985). However, the size of the phloem and vascular bundles is not the only constraint to grain filling, as an increased number of large vascular bundles entering the base of primary branches ensured better grain filling in some cultivars, but not in others (Kato, 2008). Sikder and Das Gupta (1976) suggested that growth is reduced in the spikelets on secondary branches because of unsuccessful competition for the limited pool of assimilates, while Egli and Bruening (2003) proposed that assimilate supply was the dominant factor determining seed set and grain number in crops. However, the possibility that supply of substrates discriminates between the spikelets on the secondary and primary branches of the panicle has been discounted as a cause of variation in spikelet growth and development by Mohapatra and Sahu (1991) and Yang and Zhang (2010). Vergara (1987) also reported that many spikelets in the rice panicle do not develop into high-density grains despite the presence of sufficient carbohydrates. Because unused assimilate accumulates in the inferior basal spikelets of the rice panicle, they exhibit higher callusing ability in the anther culture than the superior apical spikelets (Afza et al., 2000). Thus, it is necessary to improve the sink efficiency of the spikelets on the secondary branches and maximize the use of available assimilates to attain the yield potential of rice (Mohapatra et al., 1993). While an increase of primary branches of the panicle would be most advantageous for increasing the number of high-density grains (Padmaja Rao, 1989), there is scope for enhancing grain filling of the spikelets located on the secondary branches by manipulation of assimilate utilization.

4.2. Starch biosynthesis While starch contributes 80–90% of the final dry weight of an unpolished grain (Yoshida, 1972), sucrose is the major phloem solute which is transported to the developing rice seeds. Subsequent to loading in the source

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organ, sucrose moves by a hydrostatic pressure-gradient-induced mass flow to reach the sink. The processes of loading and unloading of the phloem sucrose are energy-dependent in rice. At the sink, unloading of sucrose depends on sink strength converting the material first into monosaccharides and later into starch. Loading of sucrose into the phloem at the source and its unloading at the sink are dependent on the proton motive force generated by HþATPase. HþATPase hydrolyses ATP to drive the sucrose–Hþ symporter (Taiz and Zeiger, 2002). Colocalization of both the transporters in the plasma membrane of sieve elements, the nucellus of pericarp and the aleurone layer of the endosperm (Furbank et al., 2001; Langhans et al., 2001), confirms close coupling of action in the transport of sucrose across the cell membrane from symplast to apoplast and vice versa. While sucrose– Hþ symporter (OsSUT1) controls loading into the phloem at the source, coordinated regulation of the symporter with cell wall invertases and monosaccharide transporters is often essential in the sink tissue for unloading and storage (Lim et al., 2006). Kuanar et al. (2010) measured the concentration of assimilates in the apoplasmic space of the developing rice caryopsis and found that it was positively correlated with endosperm cell number and grain weight. It was suggested that the concentration of apoplasmic assimilates could be an indicator of the sink-filling capacity of the caryopsis. Grain filling is impaired when the action of the sucrose transporter gene, OsSUT1, is blocked by antisense suppression (Scoefield et al., 2002). Sucrose partitioned into the endosperm is stored in the form of starch through a pathway of starch biosynthesis which is unique in cereal endosperm. The enzyme isoforms required for starch biosynthesis in rice are not found in other cereal tissues or noncereal plants ( James et al., 2003). Additionally, optimal activity of enzymes processing the incoming sucrose for starch synthesis is required for grain filling. Grain filling and the grain quality of the inferior spikelets of the rice panicle can be affected by the activity of the enzymes of sucrose metabolism in the endosperm, and the enzyme action can determine the sink strength of the endosperm. There are 33 enzymes involved in the carbohydrate metabolism of developing rice endosperm (Nakamura et al., 1989). However, only four of them, namely, sucrose synthase (EC 2.4.1.13 SUS), adenine diphosphoglucose pyrophosphorylase (EC 2.7.7.27, AGPase), starch synthase (EC 2.4.1.21 StSase), and starch branching enzyme (EC 2.4.1.18, BE), are believed to play key roles in the processes that determine starch quality and grain filling (Umemoto et al., 1994; Yang et al., 2001a). Intensive research on the function of individual enzymes has provided an insight into how the amylose and amylopectins of rice starch are synthesized and distributed, and ultimately how grain quality is determined. SUS acts on the incoming sucrose as the first step of starch synthesis (Kato, 1995; Patel and Mohapatra, 1996; Perez et al., 1975). In rice, endosperm SUS activity is

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considered as a potential indicator of high grain yield (Counce and Gravois, 2006). Activity of the enzyme is poor in the inferior spikelets compared to the superior spikelets (Patel and Mohapatra, 1996), and it is positively linked to the strength of the developing grain to accept sucrose (Liang et al., 2001; Naik and Mohapatra, 2000; Yang et al., 2003) and convert it into fructose and uridine diphosphate glucose. Although sucrose can be catalyzed into glucose and fructose by the action of invertase, SUS is the predominant enzyme during rice endosperm development (Patel and Mohapatra, 1996). UDPglucose is further metabolized to glucose-1-phosphate by phosphorylase. Glucose-1-phosphate becomes the substrate for AGPase action (Vandeputte and Delcour, 2004). AGPase catalyzes the conversion of glucose-1-phosphate and ATP into ADPglucose and inorganic pyrophosphate. Formation of the former compound is the first committed step of the starch biosynthesis pathway. Smidansky et al. (2003) reported that increased endosperm AGPase activity stimulates seed setting in the inferior spikelets of rice, increasing the grain yield by 20%, while Kato et al. (2007) suggested that sink-directed phloem transport of sucrose and improved grain filling is promoted by high activity of AGPase in the developing endosperm. The glucose moiety of ADPglucose is added to extend the chain length of amylose or amylopectin, the two major components of the starch, by the establishment of a-1, 4-glucosidic linkage to the nonreducing end of the aglucan primer by the action of soluble- and granule-bound forms of starch synthase (SS; Nakamura and Yuki, 1992; Nakamura et al., 1989). The elongation reactions for the a-1, 4 chain of amylose and amylopectin are controlled by a granule-bound form of SS and a soluble form of SS, respectively. Greater emphasis has been given to the activity of the former compared to the latter in the regulation of grain development of rice, because the amylose content and grain quality of superior spikelets are much higher than their inferior counterparts (Matsue et al., 1995). Baun et al. (1970) found that the granule-bound SS may be responsible for the integrity of amylose in the developing starch granule; the enzyme increases its activity for 21 days after flowering, equivalent to the grain-hardening stage. Similarly, Umemoto and Terashima (2002) reported that the activity of granule-bound SS is an important determinant of amylose content for low amylose cultivars, but not for high amylose cultivars. The activity of the enzyme is poor in the inferior caryopses compared to the superior caryopses of the rice panicle, and the low activity of the enzyme is related to reduced amylose content of the former (Umemoto et al., 1994). Similarly, japonica rice that has a better grain-filling ability exhibits higher specific activity of the enzyme compared to indica rice. Recent Chinese research has also revealed that poor expression of the granule-bound SS enzyme is responsible for low grain amylose content and that it can be improved by chemical mutation ( Jeng et al., 2007). The role of three more enzymes in starch biosynthesis, starch debranching enzyme, starch phosphorylase, and starch

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disproportionating enzyme (discussed in Section 4.3), has not been studied in relation to the differential pattern of grain filling between inferior and superior spikelets.

4.3. Expression profile of the genes regulating the activity of starch biosynthesis enzymes The expression pattern of both SUS and AGPase genes is lower in the developing inferior spikelets compared to the superior spikelets of the rice panicle during kernel development (Ishimaru et al., 2005). Current research indicates that six genes comprise the rice SUS gene family (Hirose et al., 2008). While SUS1 and SUS2 are more involved in the regulation of vegetative growth, SUS3 and SUS4 are exclusively responsible for partitioning of assimilates to the caryopsis during grain filling; the functions of the last two genes are not known. There are 27 genes controlling the activity of the other six enzymes in the starch synthesis pathway, namely, AGPase, SS, starch branching enzyme, starch debranching enzyme, starch phosphorylase, and starch disproportionating enzyme; the mode of expression of the genes is tissue- and developmental stage-specific (Ohdan et al., 2005). The expression profile of the genes is divided into four groups. Group 1 genes are expressed very early during grain development and involve synthesis of glucan primers for initiation of starch biosynthesis, group 2 genes are expressed throughout endosperm development, group 3 genes are initiated when starch biosynthesis occurs in the endosperm, and group 4 genes have low activity and control starch biosynthesis of the pericarp. The first enzyme, AGPase, is heterotetrameric comprising two large and two small subunits encoded by six genes in total (Ohdan et al., 2005). Two genes, OsAGPS1 and OsAGPS2, code for the small subunits and four genes, OsAGPL1, OsAGPL2, OsAGPL3, and OsAGPL4, code for the large subunits. There are two types of granule-bound SS, namely, GBSSI and GBSSII (Ohdan et al., 2005). Amylose synthesis in the rice grain is dependent on the activity of GBSSI (Vandeputte and Delcour, 2004). GBSSI gene expression reaches its peak level at 5 days after flowering and remains high until maturity. It therefore dominates starch biosynthesis in the endosperm. In contrast, the expression of the GBSSII gene is very poor throughout starch biosynthesis. Soluble-SS is classified into four types, namely, starch synthase I (SSI), starch synthase II (SSII), starch synthase III (SSIII), and starch synthase IV (SSIV) (Hirose and Terao, 2004; Kosar-Hashemi et al., 2007; Ohdan et al., 2005). In total, eight genes control the expression of these isoforms of SS in rice (Ohdan et al., 2005). SSI is the major form of SS, its activity is very high during the first few days after flowering and remains high up to the grain mid-filling stage; one gene (OsSSI) regulates the expression of this enzyme. SSII is coded by three genes, (OsSSIIa, OsSSIIb, OsSSIIc), while SSIII

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(OsSSIIIa, OsSSIIIb) and SSIV (OsSSIVa, OsSSIVb) have two genes each (Hirose and Terao, 2004). SSIIa and SSIIIa activities reach a climax 5–7 days after flowering and remain high later during grain filling (Ohdan et al., 2005). In contrast, the activity of SSIIIb is high at the start of seed formation, but decreases significantly later. SSIVb transcripts an increase up to 5 days after flowering and then decrease gradually. Compared to SSI, SSIIa, or SSIIIa, the transcripts of SSIIIb and SSIVb are much lower. The rest of the SS genes (SSIIb, SSIIc, SSIVa) are poorly expressed; their molecular expression is high during the first 5 days after flowering and low during the residual part of the grain-filling period. Ohdan et al. (2005) also studied the expression pattern of genes encoding the starch branching enzyme, starch debranching enzyme, starch phosphorylase, and starch disproportionating enzymes during seed development, but there are few reports correlating the activity of the enzymes to differential action of starch synthesis in the endosperm of rice seeds that vary in grain quality.

4.4. Hormonal regulation of spikelet development While physiological investigations undertaken into the cause of the strong metabolic dominance of the apical spikelets in grain filling and the inhibition of the inferior basal spikelets in the rice panicle have discounted the possibility of a poor assimilate supply to the inferior spikelets, Mohapatra and Sahu (1991) and Mohapatra et al. (1993) have suggested that manipulation of spikelet development with hormones or external growth regulators may be an option for improved partitioning of assimilates in favor of the inferior spikelets. After emergence, the distal spikelets quickly produce anthers, and growth inhibitors produced in the process suppress the development of other spikelets. Since the spikelet at the tip of a branch reaches anthesis (and the capacity to produce inhibitor) first, the penultimate spikelet is the most suppressed, and the order of dominance recedes in a sequence to the base (Mohapatra et al., 1993). Initially, the research on hormones concentrated on the positive manipulation of seed growth. The developing seeds are a rich source of cytokinins (Emery and Atkins, 2006; Morris, 1997) that boost seed growth through improved cell division. In the developing seeds of rice and wheat, the cytokinin content exhibits a transient increase immediately after flowering, and the high concentration of the hormone could enhance the activities of cell-cycle genes (Morris, 1997; Morris et al., 1993). An increased number of cells provide increased sink capacity for storage of assimilates. Additionally, cytokinins improve phloem unloading in the developing seeds (Clifford et al., 1986). In addition to cytokinins, abscisic acid (ABA), indole acetic acid (IAA), and gibberellic acid (GA) are also involved in the regulation of grain development (Davies, 1987). However, the specific action of these hormones in the seed development of inferior basal spikelets of rice has not been fully investigated.

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Patel and Mohapatra (1992) found that application of GA and kinetin improved growth and development more on the basal branches than on the apical branches and tended to reduce heterogeneity in the architecture of the indica rice panicle (Yang et al., 2002b). Cell number and cell division of the rice endosperm are regulated by cytokinin levels in the endosperm. In contrast, IAA accelerated growth of the spikelets on the apical branches only and increased the heterogeneity of development between apical and basal spikelets. The role of hormones in grain development of rice was further tested in six contrasting rice genotypes of indica inbreds and tropical japonica/indica hybrid lines at the International Rice Research Institute, The Philippines, by measuring the intrinsic levels of zeatin, zeatin ribosides, IAA, and GA of grains and roots at different stages of grain filling (Yang et al., 2000). While the percentage of filled grains to total grains of the cultivars did not correlate with GA or IAA, changes in zeatin and zeatin riboside contents exhibited a significant relationship with the grain-filling pattern of both superior and inferior spikelets of all cultivars. Zhao et al. (2007) also studied the role of hormones in six rice cultivars, including three two-line hybrid rice combinations showing differences in seed set and grain filling. They attributed poor plumpness and the slow rate of filling of the inferior grains to the low contents of zeatin, zeatin riboside, IAA, and ABA and the high rate of evolution of ethylene in the inferior grains. Cultural conditions also vary the grain-filling pattern in rice, and the poor filling of the inferior spikelets arising from cultural conditions is associated with low contents of zeatin riboside and IAA (Xu et al., 2007). However, ABA levels in these studies were higher in the inferior spikelet, leading Xu et al. (2007) to suggest that the shortened grain-filling period of inferior grain is related to increased ABA and reduced IAA levels in the grains. More recently, this group of researchers (Zhang et al., 2009a) reported that inferior spikelets of japonica/indica hybrids possess a slower rate of grain filling and endosperm cell division than the indica/indica hybrids, and both of these functions were positively and significantly correlated with zeatin, zeatin ribosides, and ABA contents of the developing grains. The net development of a plant organ is regulated by a balance between hormones that promote and those that inhibit development. In the context of spikelet development in rice, the hormone balance becomes crucial for survival when a spikelet is disadvantaged because of its temporal or spatial location on the panicle axis. It is possible that application of GA, cytokinins, or IAA may increase the ratio between hormones that promote and those that inhibit the grain filling of inferior spikelets. However, the role of inhibitory hormones, such as ABA or ethylene, has not been studied as extensively as that of promoter hormones. In rice, the flag leaf and the two leaves below the flag produce considerable ethylene during grain filling (Debata and Murty, 1983; Khan and Choudhury, 1992), and the ethylene production of the leaves exceeds that of the panicle (Saka et al., 1992). Similar

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ethylene emissions from the leaves and ear were also reported in wheat (Beltrano et al., 1994; Labrana et al., 1991). Spikelets in the lower part of the panicle that are confined in the flag leaf sheath for a longer period may be subjected to the inhibitory action of ethylene more than those in the upper part of the rice panicle. This concept was tested by following the effects of chemical treatments that either inhibited or encouraged ethylene action on grain development in rice (Mohapatra et al., 2000). Application of the ethylene inhibitors cobalt, silver, and 1-aminoethoxyvinyl glycine (AVG) improved the growth and development of the inferior spikelets on basal branches of the panicle, while application of the ethylene promoters, 1-aminocyclopropane1-carboxylic acid, or 2-chloroethylephosphonic acid (CEPA), inhibited the growth and development of these spikelets. The ethylene inhibitors improved starch biosynthesis and the activity of sucrose synthase and invertase enzymes only in the kernels of inferior spikelets, whereas CEPA application had the opposite effect because of enhanced ethylene production (Naik and Mohapatra, 2000). The inferior basal spikelets produced more ethylene than did the superior apical spikelets (Kuanar et al., 2010; Mohapatra and Mohapatra, 2005), and the high ethylene accelerated the senescence of the pericarp (Mohapatra and Mohapatra, 2006), retarded the development of male gametophytes (Naik and Mohapatra, 1999), diminished the activity of the starch-synthesizing enzymes, AGPase and sucrose synthase (Mohapatra et al., 2009), increased chalkiness and decreased the quality of grains (Yang et al., 2007a), and reduced the rate of cell division and starch biosynthesis, resulting in the accumulation of unused sugars in the endosperm (Panda et al., 2009) during grain filling. Ethylene accumulation in the boot of the flag leaf sheath significantly decreased grain filling in rice (Mohapatra and Mohapatra, 2006). Additionally, the compact arrangement of spikelets in the panicle axis increased ethylene production to the detriment of grain filling (Panda et al., 2009), and the extended exposure to ethylene inside the boot of the flag leaf sheath worsens the situation further for the late-emerging spikelets on the proximal part of the panicle. Yang et al. (2006a) accepted the adverse effect of ethylene on endosperm cell division and cell number and ultimately grain filling, and proposed that the antagonistic interaction between ethylene and ABA may be involved in mediating the postflowering growth and development of rice spikelets. The low ABA content of the endosperm inhibited the grain filling of inferior spikelets of rice and exogenous application has been shown to alleviate the inhibition (Zhang et al., 2009a). ABA application promoted endosperm growth by improving the assimilate partitioning to grains (Kato and Takeda, 1993; Kato et al., 1993; Yang et al., 2002a, 2006b). This has led Yang and Zhang (2010) to suggest that controlled soil drying in the mid- to late-grain-filling stages to initiate senescence and induce assimilate remobilization of stored carbohydrates can lead to improved grain filling of inferior spikelets and increased harvest index (Yang et al., 2007b).

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5. Is Manipulation of Apical Dominance Crucial for Grain Yield Improvement? Domesticated rice, Oryza sativa, originated in the monsoonal flood plains of Asia from the wild progenitor Oryza rufipogon; the presence of a continuous array of morphological intergrades between wild and cultivated forms in the Jeypore tract of Orissa bears testimony to this proposition (Oka, 1991). An undulating land surface with deep swamps and temporary marshes on higher parts of the landscape became the habitat of the diverse range of rice ecotypes, with annual types in the seasonally dry upland areas and perennial types in the swamps. The erratic pattern and distribution of rainfall might have further increased the survival of different rice ecotypes. With such variable conditions, the production of many more reproductive units (spikelets) than are usually taken to maturity was likely an important strategy for survival/adaptation in rice (Stephenson, 1981). A heterogeneous panicle architecture containing spikelets temporally and spatially segregated from one another could be an important evolutionary trait, enabling the plant to salvage some spikelets by delaying their development when unfavorable weather coincided with a critical stage of spikelet development. Apical dominance, regulated by the balance of promotive and inhibitory hormones in the nascent juvenile organs, is the best possible way of segregating the growth of individual reproductive units on the panicle axis in terms of the time scale for development and discarding spikelets in excess of resource capacity in the particular environment. While homogeneous architecture may be a useful trait under stress-free situations, it could result in loss of all the reproductive units in unfavorable conditions. With apical dominance, the shoot tip controls the shoot branching pattern by production of IAA, which in turn, regulates cytokinin levels, transport, and action (Bangerth, 1989; Sachs and Thimann, 1967). The role of cytokinins as a second signal has been corroborated by decapitation of the apical bud that removes the source of endogenous IAA and increases the availability of cytokinins in the stem, xylem sap (Bangerth, 1994; Li et al., 1995), and axillary buds by increasing the expression of adenosine phosphateisopentenyl transferase gene, which encodes a key enzyme in cytokinin biosynthesis (Tanaka et al., 2006). In contrast, the increase of IAA inhibits cytokinin synthesis (Nordstrom et al., 2004). More recently, it has been suggested that a shoot multiplication signal is involved in apical dominance (Beveridge, 2006; Dunn et al., 2006). In pea, RAMOSUS branching genes control the synthesis and perception of this signal, a strigolactone or a product of strigolactone (Ferguson and Beveridge, 2009). This branch inhibitory signal is synthesized in the shoot and roots, and IAA supply

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from the apical bud controls its availability in the stem and developing axillary branches (Dunn et al., 2006). While most of the experimental work relating to hormone control of branching patterns and apical dominance has been conducted on dicotyledonous species, monocotyledonous species have received little attention. Harrison and Kaufman (1984) reported that IAA, ABA, and ethylene could inhibit tiller bud release in oats by restricting cytokinin transport and promoting its catabolism. Kinetin-promoted tiller bud swelling and elongation was inhibited by ethylene or IAA application (Harrison and Kaufman, 1982). Estimation of endogenous levels of IAA and cytokinins supported the proposition that apical dominance of oats is regulated by a balance of IAA and cytokinins, with the ratio decreasing during tiller bud release due to an increase in the level of cytokinins (Harrison and Kaufman, 1983). With sequencing of the rice genome in the International Rice Genome Sequencing Project (2005), the genes regulating agronomically important traits like tiller and spikelet numbers, grain size, and plant height have been identified, but the mechanisms that regulate each trait have not been characterized (Sakamoto and Matsuoka, 2008). Knowledge of the genes and mechanisms controlling intergrain apical dominance on assimilates partitioning within the inflorescence is largely unknown. In rice, each culm bears a single terminal flowering inflorescence, with strong apical dominance inhibiting the development of axillary reproductive structures. Within the inflorescence, intergrain apical dominance regulates the growth of individual spikelets at the various nodes. Studies of apical dominance have focused on intact, decapitated, or in vitro systems. Ontogenetic studies and evaluation of metabolites in individual branches of the panicle have revealed that the gradient in growth and development between the apical and the basal parts of the intact panicle results from the heterogeneous architecture of the panicle (Mohapatra and Sahu, 1991; Xu and Vergara, 1986). Studies on excision of a part of the developing panicle showed that the growth and development of the inferior spikelets is amenable to physiological manipulation that reduces the heterogeneity of spikelet development and improves grain filling. Removal of some of the primary branches from the axis encouraged partitioning of carbon to residual spikelets of the panicle and improved the grain-filling percentage compared to uncut panicles (Mohapatra et al., 2004). Similarly, grain filling of inferior spikelets improved significantly when dominant spikelets of the primary branches were removed (Kato, 2004). Studies on exogenous treatments and endogenous action of hormones reviewed in Section 4.4 have clarified the physiological mechanisms involved in apical dominance in rice. Yang et al. (2000) showed that high IAA levels in the sink lead to high cytokinin levels in the grain and stimulate the partitioning of assimilates to the grain. While exogenous IAA treatment enhanced the growth of superior spikelets and depressed the growth of inferior spikelets, resulting in increased heterogeneity in spikelet growth and development of the

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panicle, applications of kinetin and GA stimulated spikelet growth and development more on the inferior proximal branches, improved homogeneity among grains, and increased the final grain yield (Patel and Mohapatra, 1992). The role of growth-retarding hormones like ABA and ethylene in the regulation of apical dominance is also emphasized in the literature. ABA in the developing grains stimulated assimilate accumulation from the prestored reserves by simulating the effects of water stress (Kato and Takeda, 1993; Yang et al., 2001b), while low levels of ABA cytokinins and IAA in the inferior spikelets restricted their growth (Zhang et al., 2009a). The role of ethylene in the regulation of intergrain signaling is a recent addition to the role of hormones in grain development. The concentration of ethylene is high in the basal branches, much to the detriment of grain filling. Temporal ethylene production is high around flowering in rice spikelets irrespective of their position on the panicle (Mohapatra and Mohapatra, 2005; Naik and Mohapatra, 2000). As the apical spikelets reach flowering nearly a week ahead of the basal spikelets (Mohapatra et al., 1993), the early production of ethylene could have an inhibitory effect on the growth and development of the basal spikelets, simulating apical dominance (Panda et al., 2009; Zhang et al., 2009b). It has been shown that the action of ethylene on grain filling counters that of ABA (Yang et al., 2006a), but is similar to root elongation of maize which is maintained under stress by ABA that restricts ethylene production (Spollen et al., 2000). However, this concept has been challenged recently by Kim et al. (2009) who reported that increased jasmonate concentration during drought stress elevated the production of ABA in rice, leading to alteration of spikelet development and loss of grain yield. In an effort to raise the yield potential of the NPT of rice, priority has been given to selection for low tillering and large panicle size (Kim and Vergara, 1992). Apical dominance is encouraged during vegetative growth in order to restrict the tiller number, but is reduced in the reproductive phase in order to allow production of a large number of spikelets competent to bear grains. Breeding has resulted in pyramiding of these two desired traits in the NPT (Peng et al., 1999; Virk et al., 2004). However, the objective of a high grain yield was not achieved because assimilate transport was not maintained to the growing sinks and the late-initiated tillers failed to thrive and died prematurely (Mohapatra and Kariali, 2008). We suggest that tiller dominance could be increased by inducing a hormonal signal from the early-formed tillers to induce early senescence of the late-formed tillers. However, the manipulation of apical dominance of the spikelets is more complicated. Yamagishi et al. (1996) showed that reduced apical dominance leading to uniform distribution of assimilates was the primary cause of poor grain filling in the NPT rice with large panicles. Thus, achievement of homogeneity in spikelet development at the cost of sacrificing the heterogeneous architecture of the rice panicle may not achieve the goal of breaking the grain-yield barrier in the newly developed rice lines with

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large panicles unless we know how to manipulate flower development with hormones and the corresponding gene expression. Chung et al. (1994) reported that the OsMADS1 gene is responsible for flower induction and reduced apical dominance in rice. This gene is only expressed in the floral organs. Empirical evidence linking expression of this gene to the hormone balance is lacking, but the evidence mentioned in Section 4.4 indicates that the inflorescence architecture of rice is amenable to modification by manipulation of the factors affecting hormone levels.

6. Suggestions for Modification of Apical Dominance Until recently, there has been no comprehensive understanding of either the physiology or genetics of apical dominance in grasses, or the use of such traits for improvement of grain yield (Morgan et al., 2002). While models by Dunn et al. (2006) and Ferguson and Beveridge (2009) have been developed based on experiments mostly with the pea plant, McSteen (2009) proposed a model for the role of hormones in axillary meristem initiation and outgrowth during both the vegetative phase and inflorescence branching of grasses. We propose a model in Figure 2 for interspikelet apical dominance within rice panicles that is in agreement with the evidence and the models referred to above. The molecular biology of hormone action is excluded from this model because of insufficient information. The model suggests that IAA traveling basipetally in the rachis from dominant spikelets inhibits the growth of inferior spikelets, while cytokinin moving acropetally promotes the growth of the latter. Both cytokinin and GA stimulate cell division and elongation. Age, nutrients, and decapitation encourage release from apical dominance and make the inferior spikelets responsive to hormone action. Dominant spikelets reach flowering and pollination early and produce ethylene, which is counterproductive to the action of cytokinins or GA. The length of time that the panicle is retained inside the boot of the flag leaf sheath, the compact architecture of the panicle as well as exposure to environmental stresses—all increase ethylene production. Environmental stresses also stimulate ABA production for the benefit of assimilate remobilization and resultant growth of the spikelet. Inclement weather can also limit current photosynthesis and assimilate production to the detriment of grain filling. At the same time, in order to sustain filling of spikelets in the large panicles of modern rice, we suggest a measure of controlled apical dominance, to produce a responsive sink with more spikelets, instead of a strong apical dominance or the absence of dominance, resulting in either heterogeneous or homogeneous architecture, respectively. The number of such spikelets would be determined by the source capacity for assimilate

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Superior spikelet (strong sink)

Roots

Compact panicle architecture or long period of spikelet retention inside the boot

Strigolactone IAA

GA

Environmental stress

Early anthesis Current photosynthesis

ABA Cytokinin Age Nutrients Decapitation

Ethylene

Remobilisation of reserve

Assimilates

Inferior spikelet (weak sink)

Responsive sink

Cell multiplication and elongation

Grain filling

Arrowhead lines indicate promotion and flat ended lines indicate inhibition.

Figure 2 Schematic of the factors influencing the development of superior and inferior spikelets on the rice panicle.

production (photosynthesis and remobilization of reserves) in a particular environment and the sink strength (balance of hormones). Since the growth of spikelets can be managed by decapitation, chemical application, and exposure to environmental conditions, and germplasm is available for variation in panicle architecture (Protection of Plant Varieties and Farmers Right Authority, 2007), we suggest that a new ideotype with many spikelets with high-quality grains can be developed by gene manipulation or breeding.

ACKNOWLEDGMENTS This work is supported by the Emeritus Scientist Scheme awarded to P. K. M. by the Council of Scientific and Industrial Research, Government of India, New Delhi. Professor Mohapatra was the recipient of the Yoshida Award for 2010 given by International Rice Research Institute, Philippines for significant contribution to rice physiology.

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