Progress and perspective on drought and salt stress tolerance in cotton

Industrial Crops & Products 130 (2019) 118–129

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Industrial Crops & Products journal homepage: www.elsevier.com/locate/indcrop

Progress and perspective on drought and salt stress tolerance in cotton a

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Abdelraheem Abdelraheem , Nardana Esmaeili , Mary O’Connell , Jinfa Zhang a b

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Department of Plant and Environmental Sciences, New Mexico State University, Las Cruces, NM, 88003, USA Department of Biological Sciences, Texas Tech University, Lubbock, TX, 79409, USA

A R T I C LE I N FO

A B S T R A C T

Keywords: Cotton Gossypium hirsutum Gossypium barbadense Drought tolerance Salt tolerance Review

Drought stress, caused by lack of precipitation or irrigation, is one of the most challenging problems in crop production in the US and worldwide. Drought alone affects 45% of the world’s agricultural land, further, 19.5% of irrigated agricultural lands are considered saline. A combination of two or more abiotic stresses, such as drought and salinity results in more yield loss than a single stress. Drought along with salinization is expected to cause up to 50% of arable land loss worldwide. Development of drought and/or salt stress tolerant cultivars represents one of the most practical solutions. Genetic variation in abiotic stress tolerance exists within Upland cotton (Gossypium hirsutum L.); however, most if not all Upland cultivars have been developed under normal well-watered and non-saline conditions. Pima, Sea-Island or Egyptian cotton (G. barbadense L.), carries some level of tolerance to abioitc stresses due to their origin near sea-coasts, and this tolerance can be transferred to Upland cotton by interspecific introgression. Although drought and salt stress tolerances are presumed to be interconnected, the genetic basis is not fully understood due to complexity of the stress resistance and difficulties in phenotyping. The objective of this review was to summarize the progress in screening methodology, resistance germplasm sources, inheritance, biochemical and molecular aspects, transgenic approaches, and quantitative trait loci (QTL) for drought and salt stress tolerance in cotton. In the last 10–15 years, significant progress has been made in understanding the genetic basis of drought and salt tolerance through QTL mapping using molecular markers on biparental and multi-parental populations and natural populations. Numerous drought or salt responsive genes have been identified, some of which include those commonly associated with drought or salt tolerance in other plants and are used in transgenic approaches for enhancement of abiotic stress tolerance. However, none of these genes have been utilized in commercial cotton breeding programs, and no abiotic stress tolerance QTL has been used in cotton breeding through marker-assisted selection (MAS). More and larger permanent intra-specific and interspecific mapping populations using diverse and multiple parents should be developed. These populations are necessary for repeated phenotyping for abiotic stress tolerance and for high resolution mapping of QTL using genome-wide SNP markers and for MAS to transfer tolerance genes to highyielding cultivars. Further, quick, reliable and high throughput screening methods applicable for large scale populations need to be developed to improve the reliability and scale of phenotyping of the cotton germplasm in these populations for drought and salt stress tolerance.

1. Introduction Cotton (Gossypium spp.) is the most important fiber crop and an important oilseed crop, providing 35% of the total fiber used worldwide (USDA-ERS, 2017a). Around 29.5 million hectares of cotton were grown in 2016–2017 worldwide, with a total production of 106.49 million bales in 2017 (USDA-ERS, 2017b). As cotton is grown in warm climates such as tropical and subtropical regions, production occurs in more than 80 countries, and cotton is a commercially leading crop in more than 30 of those countries. In 2016–2017, China was the largest raw cotton producer, followed by India, the United States, Pakistan, and ⁎

Brazil, producing 30.50, 27.00, 20.90, 8.25, and 6.50 million bales, respectively. These five countries together produce more than 2/3 of the world’s cotton fibers (USDA-NASS, 2018). The cotton genus (Gossypium spp.) includes about 50 species distributed in arid and semi-arid regions of tropics and sub-tropics, of which 45 species are diploids and five are tetraploids (Wendel and Grover, 2015). The diploid species (2n = 2x = 26) are grouped into eight genome groups, forming three major lineages corresponding to three continents: Australia (C, G, and K genomes), the Americas (D genome), and Asia/Africa/Arabia (A, B, E, and F genomes) (Stewart, 1994; Percival et al., 1999). Five species are alloteratploids (AD,

Corresponding author. E-mail address: [email protected] (J. Zhang).

https://doi.org/10.1016/j.indcrop.2018.12.070 Received 25 October 2018; Received in revised form 12 December 2018; Accepted 21 December 2018 0926-6690/ © 2018 Published by Elsevier B.V.

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mapping of quantitative trait loci (QTL) for drought and salinity tolerance in cotton. The review represents one of the first comprehensive summaries in addressing both salt and drought stress tolerance in cotton.

2n = 4x = 52) that are assigned to (AD)1 through (AD)5 on the basis of their genome organizations. Four species have been domesticated for spin-able fibers including two Old World cotton from Asia-Africa, G. herbaceum L.-A1, G. arboretum L.-A2, and two New World cotton from Americas, G. hirsutum L.-(AD)1 and G. barbadense L.- (AD)2. The most widely cultivated cotton is G. hirsutum, also known as Upland, short or medium staple Mexican cotton. This type is grown in 95% of the cotton acreage in 17 U.S. southern states from Virginia to California and accounts for more than 97% of the U.S. cotton production (USDA-ERS, 2018). Upland cotton is also grown in more than 80 countries worldwide because of its high yield potential and wide adaptability. G. barbadense, known as American Pima, Egyptian or Sea-Island cotton, produces extra-long staple or extra-fine quality fibers that contribute to less than 5% of the world cotton production. However, Pima cotton is only grown in four U.S. states (southwest Texas, southern New Mexico, Arizona, and California) and a few other countries (such as Egypt, Israel, Sudan, China, and India). This restricted production is due to the low yield and narrow adaption of this type of cotton. G. barbadense originated in the coastal areas of Peru and may have selected for genes for salinity and drought tolerance. G. barbadense is also resistant to Verticillium wilt and thrips (Adams, 2011; Ashraf, 2002; Campbell et al., 2010; Gorham et al., 2010; Tiwari et al., 2013b). Thus, G. barbadense is more tolerant to abiotic and biotic stresses than Upland cotton. The world’s population is rapidly increasing, and is expected to reach nine billion by 2050 (FAO, 2009), and the climate is also changing. Abiotic and biotic stresses are the major challenges in crop production worldwide, and climate change will likely lead to more severe abiotic and biotic stress conditions. Considering the high demands for food, fresh water, fibers, and bio-energy, it is imperative to increase crop yields by at least 40% in arid and semi-arid areas (Nakashima et al., 2014; Shaar-Moshe et al., 2017). Therefore, crop production must be tailored for development of climate-resilient crops including stresstolerant crops to sustain world agricultural production. Abiotic stress is defined as the negative impact of non-living factors on living organisms in a specific environment such as crop plants grown in field conditions. Abiotic stresses, such as drought, salinity, high temperatures, waterlogging and other environmental extremes are the major causes of reduced plant growth and yield (Acquaah, 2012). Drought alone affects 45% of the world’s agricultural land; furthermore, 19.5% of the irrigated agricultural lands are considered saline (Reis et al., 2012; Flowers and Yeo, 1995). A combination of two or more abiotic stresses, such as drought and salinity, will result in more yield loss than a single stress (Mittler, 2006). In 2015, USDA predicted that a future decline in cotton production might occur in the presence of drought stress. Indeed, cotton industry has been affected by drought and heat stress, leading to a loss of fiber yield by 34% (Ullah et al., 2017). Wang et al. (Wang et al., 2003) reported that drought along with salinization, is expected to cause up to 50% of arable land loss in the next 40 years. For example, drought in Texas in 1998 and 2009 caused more than 500 million dollars in cotton losses (Phillips, 1998; Fannin, 2006). Drought and salt stresses are caused by lack of precipitation or irrigation and are one of the most impactful stresses in the southern parts of the U.S. as well as worldwide. Although a few studies have been done to improve cotton for abiotic stress tolerance, less than expected achievements in breeding have been made, due to limited resources of tolerant germplasm, difficulties in phenotyping, and poor understanding of the genetic basis for such a complex trait as abiotic stress tolerance. To the best of our knowledge, no cotton cultivars known as abiotic stress tolerant with high yield production and fiber quality are commercially available (Higbie et al., 2010). The objectives of this review are to summarize the recent progress in drought and salt tolerance studies with a special emphasis on studies in the genetic basis of drought and salt tolerance; screening and phenotyping for drought and salt tolerance in cotton; and biochemical and molecular aspects and

2. Effects of drought and salinity on cotton Cotton is grown in arid and semi-arid regions where drought is prevalent, but it is not considered a drought-tolerant crop (Penna et al., 1998). However, cotton is classified as a moderately salt tolerant crop with a threshold of 7.7 dS m−1 (Maas and Hoffman, 1977). In general, drought and salt affect cotton at all levels, from molecular to organismal levels, which lead to reduction in plant growth, lint yield and fiber quality. This effect varies depending on timing and intensity of salt or drought stress, the growth stage, and the species. Drought has a negative effect on all cotton growth stages; however, seedling, flowering and boll development stages are most sensitive to water deficit (Turner et al., 1986; Pace et al., 1999), while seed germination and seedling stages of cotton are most sensitive to salt stress (Munns and Tester, 2008; Munns, 2002). Drought and salt have similar impacts on cotton especially during the first phase (Munns, 2002), which is known as osmotic phase, which starts after the salt concentration around the roots is increased to the threshold level. During this phase the plant’s ability to absorb water is reduced due to high salt deposition in the soil outside the plant roots (Mahajan and Tuteja, 2005). In fact, the osmotic effect may cause removal of water from plant cells, which leads to cellular dehydration and reduction in cytosolic and vacuolar volumes in the cells. This will drive stomatal closure in the aerial portions of the plant, as well as reduced cell expansion in root tips, stem, and young leaves. All new growth is inhibited (Munns and Tester, 2008; Bartels and Sunkar, 2005). The second phase, the ionic phase, starts when salt accumulates to toxic levels in old leaves through transpiration. This is a slower process than the first phase (Munns and Tester, 2008; Munns et al., 1995) and results in a change in ion homeostasis, which can be defined as the ability of a cell or an organism to maintain internal steady stage ion concentrations under an environmental stress. Salt stress inhibits the activity of various enzymes that in turn affects the related metabolic pathways. The increased salt concentration may be due to the accumulation of salt in the cell through transpiration or through cell dehydration (Zhu, 2001). The ionic phase is specific to salt stress, resulting in senescence of mature leaves and nutrient imbalances and deficiencies (Penna et al., 1998; Munns and Tester, 2008). Moreover, the stresses in these two phases affect many morphological, physiological and biochemical processes in plants that result in growth suppression and even plant death (Munns and Tester, 2008; Zhu, 2001; Verslues et al., 2006). Differential effects of osmotic stress versus ionic stress can be distinguished because ionic effects need time to accumulate in plants (Munns and Tester, 2008). 2.1. Morpho-physiological mechanisms of cotton in response to abiotic stresses Abiotic stresses cause a wide range of morpho-physiological and biochemical changes that adversely affect cotton growth and productivity. In general, abiotic stress severely restrict cotton growth and development, such as reducing plant height, fresh and dry weights of shoots and roots, leaf area index, node number, photosynthesis, transpiration rate, stomatal conductance, yield, fiber quality, and canopy and root development (Loka et al., 2011). 2.2. Root system architecture As roots are likely the first organs to perceive drought or salt stresses, the root system plays a critical role in response to these abiotic stresses. Some plants have the ability to increase their root growth at 119

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than normal leaf type isolines, and they maintained higher leaf and turgor potentials under water stress conditions and exhibited higher photosynthetic rate under drought stress in both greenhouse and field conditions. Similar results were obtained in okra leaf type cotton plants under dryland conditions, suggesting this leaf morphology can be a component of drought resistance (Stiller et al., 2005).

early stages of abiotic stresses, which results in longer root systems able to absorb water from deeper soi. Increased root growth measured as length, weight, volume, and density of plant roots were reported to be associated with abiotic stress tolerance in crops. Crops, including cotton, can have tap roots with ten times the length of the aboveground plant height (Larcher, 2003). Interestingly, in cotton, initial or mild drought increased root length under drought conditions (Luo et al., 2016), but a longer or more severe drought reduced root length and weight. Ashraf (Adams, 2011) reported similar results under salt stress in that moderate levels of salinity increased root growth and leaf thickness. Leidi (1994) confirmed these results under either a stress induced by polyethylene glycol (PEG) or by NaCl conditions. Water deficit alters the ratio of root to shoot biomass accumulation through inhibition of shoot growth more than root growth (Ball et al., 1994). Leidi et al. (1991) reported that salinity reduced shoot weight, resulting in decreased root/shoot ratio. However, studies showed that root to shoot ratio tended to be increased under abiotic stresses (McMichael and Quisenberry, 1991). Therefore, shoot length, shoot and root fresh and dry weights, and root to shoot ratios are potential traits that can be taken into consideration when selecting cotton genotypes under abiotic stress conditions (Ashraf and Ahmad, 2000; Basal et al., 2006; Dewi, 2009). Basal et al. (2006) evaluated root growth of selected converted race stocks under drought. As a result, two converted cotton race stocks were identified with a robust rooting system and longer tap root length, higher lateral root number, greater total root dry weight, larger root weight per unit length of tap root, and greater shoot dry weight in both drought and well-watered conditions, compared to two other converted race stocks identified as non-robust.

2.4. Yield and yield component traits Several field studies have been conducted to investigate the impacts of drought or salt on lint yield, the most important final product of cotton production. There are negative correlations between physiology and/or morphological traits and yield. Although in this type of field screening, the final product can be measured, other confounding factors, such as soil type, timing and amount of rains, may also affect the results. Genotype and environment interaction are often observed. Inconsistent field results have been obtained, slowing the development of drought and/or salt tolerant cotton cultivars. (Adams 2011) evaluated an interspecific Upland × Pima backcross inbred line (BIL) population in two locations over two years. Drought treatment from a delayed irrigation decreased lint yield (by 45%), boll weight and lint percentage, as compared to a normal irrigation treatment. () evaluated an introgressed inbred line population of Upland cotton also in delayed irrigation conditions and determined the reduction due to water deficit in seedcotton yield was 48.2%; in lint yield, 41.2%; in boll weight, 40.0%; and in lint percentage, 21.0%. Levi et al. (2009) evaluated four near-isogenic lines from an Upland × Pima cotton cross under field conditions, and found that seedcotton yield under drought treatments was only 31% of that under normal irrigation conditions. Other studies (Ashraf, 2002; Maas and Hoffman, 1977; Ashraf and Ahmad, 2000) also reported up to 50% yield reduction when the salinity level was increased from 7.7 dS m−1 to 17.0 dS m-1.

2.3. Photosynthetic rate and stomatal conductance Plant production is determined by photosynthesis, which is controlled by stomata for CO2/water exchange and photosynthetic activity in mesophyll cells. Drought and salinity stresses have a direct impact on stomatal and mesophyll conductance (gm) as well as on gene expression, which results in alterations of photosynthetic metabolism (Chaves et al., 2009). It is well established that, stomatal closure caused by abiotic stress decreased CO2 intake, which results in decreased photosynthetic rate, cotton growth inhibition, and lower yield production (Chaves et al., 2002; Chastaina et al., 2014). In cotton, several reports have indicated that water stress reduces photosynthetic rates due to a combination of stomatal and non-stomatal limitations (Turner et al., 1986; Chaves et al., 2002; Lacape et al., 1998; Leidi et al., 1999). Carmo-Silva et al. (2012) evaluated four Pima genotypes (Monseratt Sea Island, Pima 32, Pima S-6 and Pima S-7) under well-watered and water-limited conditions. Stomatal closure and increased leaf temperature led to decreased CO2 uptake and inactivation of Rubisco, resulting in reduction of photosynthetic rate. However, some studies (Caemmerer et al., 2004; Xu et al., 2010) reported that stomatal conductance is not always associated with photosynthetic rate. In yet other studies, transpiration as well as photosynthesis was affected under drought conditions in cotton (Deeba et al., 2012; Li et al., 2012). Brugnoli and Lauteri (1991) demonstrated that the effect of salinity in a salt tolerant Upland cultivar was due to the reduction of stomatal conductance. Moreover, other factors such as the time of an abiotic stress, leaf type, ambient CO2 concentrations, growth stage, genotypes, and abscisic acid (ABA) concentrations have been associated with photosynthetic rate under abiotic stress conditions. Ackerson et al. (Ackerson and Krieg, 1977) reported that photosynthetic rates were affected by different times of the day (morning vs. afternoon) and leaf age. Young leaves of cotton are photosynthetically more tolerant to drought and heat stress than mature leaves even when leaves were exposed to high temperatures, e.g., > 37 °C (Chastain et al., 2016). Other studies (Pettigrew et al., 1993; Pettigrew, 2004) found that the okra and super okra leaf type cotton plants had lower stomatal conductance values

2.5. Fiber quality As fiber quality is one of the main breeding objectives in most cotton breeding and genetics programs (May and Jividen, 1999), many studies have been done under normal cotton production conditions to determine fiber quality traits such as length, strength and micronaire. However, breeding for cultivars with improved yield potentials and good fiber quality under stress conditions is becoming more important (Cattivell et al., 2008). The development of cotton fibers is mainly dependent on water, to maintain the turgor of the cells and assimilation of carbohydrates. Therefore, cotton leaves under stress conditions lose turgor and reduce photosynthesis that lead to a decrease in carbohydrate supply to developing bolls which will consequently affects the fiber development (Dhindsa et al., 1975). However, most fiber properties are reported to be less sensitive to water-deficit stress (Adams, 2011; Abdelraheem and Zhang, 2016b; Esha, 2011; Marani and Amirav, 1971) under mild to severe stress. However, under an extreme drought stress (at the water potential of -2.8 MPa), fiber length was reduced (Bennett et al., 1967). Others report that drought stress causes a significant reduction in micronaire (Esha, 2011; Marani and Amirav, 1971). Salinity has been shown to reduce lint percentage and fiber quality including fiber length, strength, and micronaire (fineness and maturity) (Ashraf and Ahmad, 2000; Korkor et al., 1974; Longenecke, 1974). However, Ye et al. (1997) observed an increased fiber length and reduced fiber fineness and elongation under soil salinity of 0.42%. The timing of a stress is one of the most important factors affecting fiber quality. While early stress during the flowering season on two Upland cotton cultivars of Acala 4–42 and Deltapine Smoothleaf had no effect on fiber quality, but if applied shortly after flowering, the stress reduced the quality of the fiber (Marani and Amirav, 1971). 120

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3. Screening techniques for drought and salt tolerance in cotton

cultivars were developed under optimum growth conditions, which unintentionally leads to reduced genetic diversity for selection of drought and salt stress tolerance in cotton. Among the four cultivated cotton species, G. barbadense carries some desirable traits such as higher levels of tolerance to biotic and abiotic stress (Zhang et al., 2014a). However, G. barbadense is planted on a very limited acreage and the tolerance traits have not been successfully transferred into commercial Upland cotton due to hybrid breakdown (Zhang et al., 2014a). Moreover, the genetic diversity of Upland is very low due to an intensive artificial selection for economically important traits during the domestication and breeding process (Abdalla et al., 2001; Wendel et al., 1992). However, some genotypic differences in abiotic stress tolerance do exist within Upland cotton. In the greenhouse, Penna et al. (1998) screened Upland genotypes for drought tolerance at the seedling stage and demonstrated that the response of Upland to drought stress ranged from tolerant to sensitive, and germplasm ‘IAC-13-1’, ‘IAC-RM4-SM5’, ‘Minas Sertaneja’, ‘Acala 1517E-1’, and ‘4521’ were more drought tolerant. Sezener et al. (2015) screened 96 Upland cotton genotypes under field conditions for two years and found that 23 genotypes were drought tolerant with higher seedcotton yields. A number of studies were conducted in the greenhouse to screen cotton germplasm for drought and salt tolerance. Abdelraheem et al. (2016b) screened 367 Upland cotton accessions for drought and salt stress tolerance in the greenhouse and identified 24 and 45 accessions tolerant to drought and salt, respectively. In addition, some accessions exhibited tolerance to both stresses. (Abdelraheem and Zhang, 2016b; Abdelraheem et al. 2015a, b; Abdelraheem et al., 2016a) further screened more than 1500 recombinant inbred lines (RILs) from different genetic mapping populations and reported that tolerance or resistance to both stresses existed in interspecific and intraspecific cotton. Barrick et al. (2015) evaluated four introgressed Upland cotton from a G. hirsutum × G. barbadense backcross inbred line population grown in two different soil types, i.e., an organic and a loam soil using 200 mM NaCl for three weeks. Data on plant height, chlorophyll content and fluorescence, leaf size, main stem node number and internode length, shoot biomass, and number of fruiting sites were collected. Genotypic variation was detected, indicating that screening cotton for salt tolerance at the seeding stage is optimum. Tiwari et al. (2013a) demonstrated that G. barabdense is more tolerant that G. hirsutum in seed germination using 200 mM NaCl. Moreover, Niu et al. (2013) used five cotton genotypes, including three Upland (‘DN 1’, ‘DP 491’, and ‘FM 989’) and two Pima (‘Pima Cobalt’ and ‘Pima S-7’) using 100 and 150 mM NaCl, and 70 and 111 mM Na2SO4 concentrations. All the genotypes had significant growth reduction compared to the nonsaline control, but no significant difference was noted between Upland and Pima in their response to salt. Sun et al. (2015) compared ‘Acala 1517-99’ and ‘PHY76 Pima’ and their interspecific crossbreeding line ‘NM Q1735-4’ in a greenhouse grown using four substrate volumetric water contents of 15, 25, 35, and 45%. At the drought stress level of 25% water content, the growth reduction in Acala 1517-99, PHY76 Pima and NM Q1735-4 for plant height was 39.2, 32.5 and 23.7%; for leaf area the reduction was 70.9, 65.8 and 34.7%; for stem diameter the reduction was 33.4, 28.1 and 22.1%; and for dry weight the reduction was 59.2, 55.6, and 15.1%, respectively. The Pima cotton was more drought tolerant than the Upland cotton, and the interspecific progeny was the most drought tolerant.

There are different ways to screen cotton germplasm for drought stress tolerance. Screening under field conditions is simple and reliable, but it is restricted by seasons, and it is labor intensive and time-consuming, specifically when screening a large number of germplasm. In cotton, some studies were conducted for drought tolerance under field conditions (Adams, 2011; Abdelraheem, 2006). In field studies for drought stress tolerance in cotton, water deficit treatments can be applied to different levels of water holding capacity at different growth stages through irrigation. Plant height, number of leaves and leaf size, and biomass (if a destructive sampling is possible) can be determined. The field experiment can be carried out through crop maturation to measure the number of fruiting branches, fruiting sites and mature bolls, boll and seed weight, lint percentage, and seedcotton and lint yields (Adams, 2011; Abdelraheem et al., 2018a; Saranga et al., 2001, 2004; Levi et al., 2009; Abdelraheem et al., 2017b). A second screening method is through pot culture based upon the soil holding capacity, which varies in soil types and is still time-consuming. However, screening germplasm for drought tolerance in the greenhouse is becoming more attractive using chemicals such as mannitol or PEG to induce osmotic stress which makes the uptake of water more difficult. Hydroponics and its modifications have been used in different crops including cotton (James and Murray, 1979; Michel, 1983; Nepomuceno et al., 1998; Nguyen et al., 2013; Abdelraheem et al., 2015a; Zhang et al., 2007) to assess drought and salinity tolerances. In contrast, screens involving soil salinity are more complex over space and time. Evaluation for salinity tolerance in the field is difficult and not accurate, because fields with a uniform salinity are usually unavailable. The soil salinity heterogeneity will result in high experimental errors, leading to little progress toward improvement in salt tolerance. Nevertheless, it is useful in screening a large number of cotton germplasm and selecting for their relative salinity tolerance if a field with uniform soil salinity can be identified. Therefore, screening germplasm using a pot culture is a useful way, in which graded salinity levels can be created by irrigating the plants with known salinity solutions. However, the physical and chemical properties of the soil vary to a large extent, so it is difficult to ensure if the plant is growing under a desired level of salinity. Therefore, hydroponics (water culture) is the most useful way in screening germplasm for salt tolerance. In hydroponics, plants are grown with a known level of salinity, so the absolute effect of salt on plant growth and the threshold concentration required to bring reduction in plant growth can be determined. Abdelraheem et al. (2015a, 2016a, b, 2018a, b) evaluated different genetic mapping populations including a multi-parent advanced generation inter-cross (MAGIC) population of Upland cotton consisting of 550 lines and an association mapping panel of 376 Upland cotton accessions for drought and salt tolerance using a hydroponic system. In these studies, seeds were sown in potting soil in pots until the second true leaves appeared. Then seedlings were transferred to a hydroponic system for salt or drought treatments using NaCl, PEG, or water. Then, plant height, fresh and dry weights of shoots and roots can be measured. The pot experiments especially using a hydroponic system will allow a better study on root growth and architecture, which has received less attention in the past because of the difficulty in extracting and evaluating roots. Also, hydroponic systems will allow investigations of the responses in older plants; in a small pot system, seedlings can only be treated for a short period of time such as 3–4 weeks.

5. Inheritance of drought and salt tolerance in cotton Due to the limited introgression of desirable traits in the early generations between interspecific Upland and Pima cotton, studying the genetic basis of abiotic stress tolerance within each species is needed. Traditional quantitative genetic designs such as diallel analysis and generation mean analysis are often employed to estimate genetic parameters such as additive effect (or variance) due to the different contributions of homozygous alleles and non-additive effects (variance)

4. Tolerance sources in cotton As stated above, there are various mechanisms for plants to cope with abiotic stresses; however, developing resistant cultivars is the best way to alleviate drought and salt stresses in cotton production. Sources of abiotic stress tolerance are very limited, because most cotton 121

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(1O2) in the cell results in oxidation of various biochemical compounds: lipids, proteins, DNA, and RNA (Tripathy and Oelmüller, 2012). However, plants have evolved antioxidative mechanisms to cope with ROS production and accumulation. These mechanisms include: (i) enzymatic components, such as catalase (CAT), ascorbate peroxidase (APX), glutathione reductase (GR), guaiacol peroxidase (GPX), dehydroascorbate reductase (DHA), and monodehydroascorbate reductase (MDAR); and (ii) non-enzymatic antioxidants, such as reduced glutathione, ascorbic acid, a-tocopherol, flavonoids, and carotenoids. Although the antioxidative mechanisms are the first choice of the plant to cope with ROS production, Zhang et al. (2014c) stated that the balance between ROS production and antioxidative enzyme activities in cotton under drought stress determines whether oxidative signaling and/or damage will occur. Ratnayaka et al. (2003) reported that, under drought stress, ROS were produced in cotton; however, the APX and GR activities also increased and plants maintained the ROS scavenging process until the plant recovered from the stress conditions. Sekmen et al. (2014) assessed the physiological and biochemical responses of two cotton cultivars (‘84-S’ and ‘M-503’) differing in drought tolerance to the combined effects of drought and heat. The sensitive cultivar 84-S had decreased activities of CAT and peroxidase (POX) during the stress condition as compared to control conditions, resulting in higher H2O2 accumulation and oxidative stress-induced lipid peroxidation. However, the drought-tolerant cultivar M-503 maintained constitutive levels of enzyme activities for superoxide dismutase (SOD) and APX and increased the levels of CAT, POX, and proline content under drought and heat stresses. Wu et al. (2015) reported that supplemental Zn significantly increased photosynthetic rate, chlorophyll a and b content, and biomass of cotton under PEG 6000. The activities of antioxidant enzymes such as CAT, APX and SOD, and non-enzymatic antioxidants such as carotenoids, reduced glutathione and ascorbic acid and osmoregulation substances such as soluble sugar, proline and soluble protein were increased, while malonaldehyde content was reduced under PEG. The capacity of scavenging ROS was improved by supplemental zinc in cotton under drought stress. Zhang et al. (2014b) reported that, increasing levels of salinity increased the activities of SOD, APX, and GR in the leaves and roots of the salt-tolerant cultivar ‘CCRI79’, but reduced the CAT activity. CAT and APX showed the greatest H2O2 scavenging activity in both leaves and roots. The authors stated that CAT and APX activities in conjunction with SOD played an essential protective role in the scavenging process. Li et al. (2010) reported that two cotton Di19 proteins (i.e., GhDi19-1 and GhDi19-2) were involved in response to salt stress and ABA signaling. In order for plants to survive under such abiotic stress conditions, a sophisticated process occurs inside the plants to coordinate the changes in release of specific endogenous molecules such as jasmonic acid, ethylene, and abscisic acid that allow plants to adapt to and/or avoid the stress (Fujita et al., 2006).

including dominance effect (or variance) due to the contribution of heterozygous alleles and epistatic effect (or variance) due to the interactions of alleles from different loci. Most studies indicate that drought tolerance in G. hirsutum is controlled by additive, dominant and epistatic genetic effects in early generations (F1, F2, and BC1). Soomro et al. (2012) reported that the mean squares of general combing ability (GCA) due to additive effects were higher than specific combing ability (SCA) due to non-additive effects for plant height, leaf area, leaf dry weight, number of bolls per plant and seedcotton yield under drought and non-drought regimes. Nasimi et al. (2016) used four drought-tolerant and four susceptible lines in a diallel analysis, which were selected from 50 accessions based on root length. Results confirmed the existence of additive and non-additive effects, but the large proportion was additive toward fiber quality traits including fiber length, strength and fineness under drought conditions. Ahmed (2007) used hybrids from four Egyptian cultivars and one Upland cotton to study the genetic effect under drought conditions. The non-additive effect was larger than the additive effects for all traits except for days to first flower. Similar results were reported for salt tolerance in Upland cotton using generation mean analysis (Ashraf and Ahmad, 2000; Nabi et al., 2010), suggesting that additive and dominant gene effects were both responsible for most of the traits with higher additive effects for fiber quality traits. Abdelraheem (2006) performed a diallel analysis using nine Egyptian cotton cultivars. A simple additive model of inheritance was adequate to explain the genetic basis of most agronomic traits including seedcotton yield, lint yield, boll weight, number of bolls plant−1, lint percent, and lint and seed indices under well-watered conditions, but dominance effects were larger than additive effects under water-limited conditions in clay and sandy soils in two different locations. Mohamed et al. (2009) and Esmail and Abdelsattar (2001) confirmed that addtive effects were more important for seedcotton yield and boll weight under normal conditions and non-additive effects uder stress conditons in a diallel crossing of six Egyptian cultivars. (Zhang et al. (2016); Zhang and Abdelraheem, 2017a; Zhang et al., 2017b) reported the detection of additive effect under control condition for yield and its components and fiber quality traits. The same trend was detected in screening for salt tolerance in Upland cotton (Gholamhossein and Thengane, 2007). Gholamhossein and Thengane (2007) reported that narrow-sense heritability estimates were high for ion concentrations and ion ratios (Na+, K+, Ca2+, K+/Na+, and Ca2+/Na+) and ranged from 0.37 to 0.48, 0.46 to 0.54, 0.54 to 0.69, 0.55 to 0.63, and 0.53 to 0.64, in the leaf tissue, root length, plant height, root length/shoot height ratio, and tolerance index, respectively, indicating the existence of additive gene effects. Tiwari et al. (2013a, b) estimated the broad-sense heritability for salt tolerance at the germination and seedling stages. Heritability in germination ranged from 0.39 to 0.43 and 0.43 to 0.69 at the seedling stage. Similar results were obtained by Abdelraheem et al. (2015a, 2018a) under salt or osmotic stress conditions in the greenhouse, and under field drought stress conditions. Results showed that heritabilities were low to moderate for yield and its components and ranged from 0.42 to 0.63. Similar trends were observed for morphological and physiological traits measured under both drought and salt stress conditions and ranged from 0.39 to 0.55 and 0.45 to 0.56, respectively. The broad-sense heritability estimates ranged from 0.69 to 0.76 for fiber quality traits under field drought stress conditions.

6.2. Sensing salt stress and signaling pathways There are unique stress specific responses and there are other responses that are common to all of the abioitc stresses: drought, salinity, heat, cold, and flooding. Once plants perceive abiotic stress signals, physiology, morphology, and development throughout plant stages are changed (Bray et al., 2000) due to the cellular response that is generated from a complex signal transduction system (Sanders et al., 2002). These signals start with stress sensors, followed by signaling pathways comprised of a network of protein-protein interactions, including interaction between transcription factor binding proteins (TFBPs), transcription factors (TFs) and promoters, and finally end with cellular responses and activation or inhibition of specific gene expression patterns. Moreover, the lack of a response to such signaling steps and gene activation will result in cellular homeostasis changes and destruction of the protein functions leading to cell death. All these could result in changes in morphology and physiology and ultimately yield loss when

6. Biochemical and molecular aspects of drought and salinity tolerance in cotton 6.1. Reactive oxygen species (ROS) and antioxidative mechanisms Abiotic stresses cause plant damage in part by inducing overproduction of reactive oxygen species (ROS), which leads to cellular damage and inhibition of physiological process in plants. The accumulation of ROS such as hydroxyl radical (HO•) and singlet oxygen 122

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cell, such as changes in the levels of Ca2+, inositol phosphates, ROS, nitric oxide (NO), or ABA. Calcium signals are transferred by three Ca2+ sensor molecules including calmodulin (CaM) and CaM-related proteins, calcium-dependent protein kinase (CDPK) and calcineurin B-like proteins (CBLs). Due to the association between calcium sensors and fiber development, genes related to CaM and CaM-related proteins have also been studied during cotton fiber elongation (Cheng et al., 2016; Tang et al., 2014). Huang et al. (2008) reported that calcium signaling was associated with fiber elongation, and Li et al. (2015) reported 41 calcium-dependent protein kinase CDPK genes in the G. raimondii genome. Moreover, genes such as GhCDPK3, GhCDPK2, GhCDPK11, GhCDPK16, GhCDPK28, GhCDPK35 and GhCDPK14 were found to be associated with drought and salt stresses in Upland cotton. These signaling pathways are associated with increased concentration of cytosolic Ca2+ that are involved in transferring these signals to a cascade of responses which ultimately result in changes in gene transcription (Deinlein et al., 2014). Transcription factors (TFs) such as GT element-binding-like proteins (GTLs) and MYBs that are activated by Ca2+/calmodulin, leucine zipper (bZIP), helix–loop–helix, calcineurin B-like proteins (CBLs), CBL-interacting protein kinases (CIPKs), and NAC families have been reported to be associated with abiotic stress tolerance in cotton and other crops. These TFs are involved in perception of the signal and the abiotic stress responsive gene expression in the signal transduction process, in which TFs activate the signaling cascade of the entire network of abiotic stress-responsive genes (Guo et al., 2016; Chen et al., 2002; Rabbani et al., 2003; Rodriguez-Uribe et al., 2011, 2014). These TFs are good candidates for improvements of cotton against abiotic stress as they regulate the expression of candidate genes related to osmotic stress caused by both drought stress and salinity. Liang et al. (2016a) reported that a bZIP TF gene, GhABF2, has been involved in the drought and salt tolerance in Arabidopsis and cotton. Several candidate genes have been used in transgenic approaches to confirm their effects in drought and salt tolerance (Bajaj et al., 1999; Umezawa et al., 2006). Huang and Liu (2006) reported a cDNA encoding G. hirsutum DRE-binding protein 1 (GhDBP1) that acts as a transcriptional repressor for DRE-mediated gene expression. (Wu et al., 2004) demonstrated that a cDNA clone, encoding a vacuolar-type Na+/ H+ antiporterGhNHX1, was isolated in response to salt stress in cotton seedlings. According to He et al. (2005), transgenic cotton engineered with AtNHX1, the Arabidopsis orthologue for GhNHX, had improved yield, biomass, and fiber quality under a high NaCl stress. Many abiotic stress responsive genes have been identified in the model plant Arabidopsis, and some have exhibited a critical role in protecting plants under abiotic stress conditions. For example, the Arabidopsis vacuolar H+-pyrophosphatase gene (AVP1) is one of the most promising genes that may be used to improve drought- and salt-tolerance in plants including cotton (Pasapula et al., 2011).

abiotic stresses are severe or persistent (Bartels and Sunkar, 2005). 6.3. Plant mechanisms to cope with osmotic stress The plant abiotic stress mechanisms against osmotic stress can be categorized into four mechanisms (Levitt, 1972). First, dehydration avoidance (DA), in which plants can maintain fundamental normal physiological processes under mild or moderate drought and salt stress conditions by adjusting certain morphological structures or growth rates such as leaf rolling and thickness to avoid the negative effects caused by drought stress (Blum, 2005). Second, dehydration tolerance (DT), in which plants maintain cellular moisture by increasing water uptake through a well-developed root system, increased water use efficiency, reducing water loss via stomatal closure, and osmotic adjustment in the presence of water shortage and also by delaying senescence (Mitra, 2001). Third, dehydration escape (DE), which is the ability of plants to complete their lifecycle in a short period of time by early flowering. In cotton, short-season cultivars are an excellent example for this mechanism (Manavalan et al., 2009). Fourth, drought recovery (DR) that refers to the plant’s ability to resume growth and gain yield after exposure to severe drought stress. Among these, DA and DT are the two major mechanisms for drought resistance; however, cotton can adapt to a variety of stressful environments by combining different categories of mechanisms to confer abiotic resistance at different developmental stages. As the nature of drought stress is dynamic and unpredictable in crop production, phenotyping drought tolerance is much more difficult than studying other stress resistances (Levitt, 1980; Kirda, 2002). In spite of difficulties in phenotyping, numerous traits in cotton have been used to study abiotic stress tolerance. In cotton, specific traits or several combined traits that are associated with dehydration avoidance and/or dehydration tolerance have been used to assess abiotic stress tolerance, and even some complex traits relevant to biomass or economic yield under stress conditions can also be used to evaluate abiotic resistance such as fresh and dry weights, plant height, and other physiologically related traits including photosynthesis, stomatal conductance and chlorophyll content (Oluoch et al., 2016; Du et al., 2017). Results suggested that root parameters including tap root length, root number, dry root weight as well as dry shoot weight and plant height and water content are good indicators for drought and salinity tolerance in cotton (Basal et al., 2006; Abdelraheem et al., 2015a, b). 6.4. Plant mechanisms to cope with ionic stress and signaling pathways Plants have developed several adaptive mechanisms under salt stress such as ion compartmentalization, ion exclusion and osmotic adjustment. Salt stress also has toxic effects on plants and decreases crop productivity. To cope with ionic stresses, plants exhibit a range of mechanisms from exclusion of Na+ to tolerance within the cells through osmotic adjustments. As a result of Na+ exclusion by roots, plants prevent Na+ from reaching toxic concentrations within leaves (Munns and Tester, 2008). Na+ is taken up by roots and transported to the shoot via the transpiration stream. Genetic engineering approach could improve this by changing plasma membrane Na+ transport processes in the root. Another mechanism is tissue tolerance in which the tissue shows tolerance to accumulation of Na+ by compartmentalization of Na+ and Cl− at the cellular and intracellular level in order to avoid toxic concentrations within the cytoplasm (Munns and Tester, 2008). When plants are subjected to ionic stress, many complex processes occur from the molecular level through biochemical and physiological responses. First, receptor proteins detect or perceive the salt stress; these proteins include, G-protein-coupled receptors, ion channels, the plasma membrane Na+/H+ antiporter SOS1 (salt overly sensitive), receptor-like kinases or histidine kinases. The major function of these proteins is to transfer signals to generate secondary signals within the

6.5. Osmotic adjustment (OA) Osmotic adjustment is associated with dehydration tolerance (DT), and it is a general mechanism for a number of abiotic stress responses. Briefly, at the cellular level the osmotic potential is maintained or increased by changes in osmolyte content, and often these changes are driven by changes in ABA content. Plants start their defense against abiotic stresses by accumulating a variety of organic and inorganic substances such as sugars, proline, mannitol, amino acids, alkaloids, and inorganic ions to increase their concentration in the cells, and reduce the osmotic potential in response to abiotic stresses (Fang and Xiong, 2015). Boyer (1982) reported that osmotic adjustment enables plants to: continue normal leaf elongation but at a reduced rate, adjust their stomatal and photosynthetic functions, maintain root system development to capture soil water, postpone leaf senescence, and achieve better dry matter accumulation and yield production under adverse conditions. In cotton, these solutes play a critical role to protect 123

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seedcotton yield, harvest index, boll weight and boll number; and fiber quality traits: fiber length, length uniformity, fineness (micronaire), strength, elongation, and color components (reflectance and yellowness). As a result, a total of 33, 46, and 79 QTL were detected for traits related to physiological traits, productivity, and fiber quality, respectively. However, only 33 QTL were detected under water-limited conditions, and only lower osmotic adjustment was found to contribute to higher seedcotton yield under drought stress, indicating the existence of a phenotypic correlation between physiological and productivity traits. These findings, along with results by Levi et al. (2009), who evaluated near-isogenic lines (NILs) under well-watered and water-limited conditions in a multi-environment field trial, indicate that improvements of polygenic traits such as yield and drought tolerance via marker-assisted backcrossing is a big challenge. Oluoch et al. (2016) screened a population of 188 F2:3 progeny derived from a cross between Upland and an accession of a wild type belonging to G. tomentosum Nutt. ex Seem for salt tolerance in a hydroponic system for two weeks at 150 mM of NaCl. A total of 11 QTL were detected on 8 chromosomes (i.e., c9, 11, 15, 16, 21, 23, 24 and 26) using 1295 simple sequence repeat (SSR) markers, 10 of which were located on the D subgenome. The same population was used to identify QTL for drought tolerance by Zheng et al. (2016) under field conditions. A total of 67 and 35 QTL were detected under water-limited and well-watered conditions, respectively. The favorable alleles to improve the traits exhibited partial or over-dominance effects. Stress tolerance QTL were found on four chromosomes c5, c8, c9, and c16, and 13 QTL clusters were found on nine chromosomes c2, c3, c5, c6, c9, c14, c15, c16, and c21. Another 277 individuals in an F2:3 population were evaluated for salt tolerance at the seedlings stage by Diouf et al. (2017) using 5178 single nucleotide polymorphic (SNP) markers. A total of 66 QTL were detected in three levels of salt treatments (0, 110, and 150 mM salt treatment) and 14 QTL were found to be consistent, each only accounting for 2.72% to 9.97% of the phenotypic variation. All the QTL results were from early segregating populations in above studies; as such, these experiments cannot be repeated. Therefore, permanent genetic mapping populations should be developed and used for multiple repeated tests. conducted a study to identify drought and salt tolerance QTL in an introgressed Upland population under greenhouse and field conditions using 1004 polymorphic DNA marker loci including 481 SNPs and 523 SSRs. A total of 165 QTL were distributed across most of the cotton chromosomes; each QTL explained 5.98–21.43 % of the phenotypic variation. Moreover, 15 common abiotic stress tolerance QTL were detected on 12 chromosomes (c1, c2, c5, c6, c8, c9, c10, c12, c20, c23, c25, and c26). Interestingly, a QTL cluster was found on chromosome c5 for plant height as measured under drought stress conditions in both the field and greenhouse and salt tolerance in the greenhouse. With the limited number of QTL detected for drought and salt tolerance in cotton, more QTL mapping for abiotic stress tolerance is needed using different strategies. First, more markers including those developed from candidate genes for abiotic responsiveness (Tiwari et al., 2013b; Abdelraheem et al., 2015b; Rodriguez-Uribe et al., 2014) and genome-wide SNP markers are needed. Genotyping-by-sequencing (GBS) has been used in different crops including cotton as a lower cost alternative approach to detect thousands of genome-wide SNP markers across multiple individuals from diverse populations (Abdelraheem and Zhang, 2016b; Elshire et al., 2011; Poland and Rife, 2012; Gore et al., 2014). Another SNP typing platform is the development and use of SNP chips to detect high level of polymorphisms. Second, permanent mapping populations should be developed and used in QTL mapping for drought and salt tolerance in cotton, as replicated experiments using the same genetic populations are important to reliably detect genetic variation and understand the genetic basis for tolerance to abiotic stress such as drought and salt based on QTL mapping. Asins (2002) indicated that progress can be made in this area using a large RIL population to determine the genetic relationship of tolerance to different stresses. For

proteins and membranes from the damage due to high concentrations of inorganic ions and oxidative damage under multiple abiotic stresses (Khan et al., 2015). Proline and glycinebetaine have been associated with decreasing harmful effects under drought stress by increasing photosynthetic rate, leaf water content and osmotic adjustments (Noreen et al., 2013; Lv et al., 2007). Moreover, transgenic cotton plants with a higher capability of accumulating glycinebetaine displayed improved drought tolerance with increased photosynthetic rates via an osmotic adjustment mechanism (Lu et al., 2013). Butt et al. (2017) reported that the overexpression of GaMYB62 L protein increased proline and chlorophyll content and seed germination rate under salt and osmotic stress, and reduced water loss by decreasing stomatal apertures. Tianet al. (Tian et al., 2016) also reported that GhCDPK1, induced under PEG conditions, resulted in increased contents of chlorophyll, proline and soluble protein, and the activities of POD and SOD, leading to increased osmotic adjustment in cotton under the PEG stress. Oosterhuis and Wullschleger (1987) evaluated Upland ‘Deltapine 41’ to investigate the magnitude of osmotic adjustment in cotton leaves and roots in response to water stress. They showed that cotton roots exhibited a much larger percentage of osmotic adjustments compared to cotton leaves. Ackerson and Hebert (1981) reported that Upland ‘Tamcot SP37’ exhibited increased osmoregulation when subjected to mid-day stress (leaf water potential of -20 bars), and photosynthetic rates were higher due to higher stomatal conductance at these low leaf water potentials. 7. Quantitative trait locus (QTL) mapping, and identification of QTL clusters and hotspots for drought and salt tolerance in cotton Molecular markers have been used to identify quantitative trait loci (QTL) responsible for improved cotton production under abiotic stress conditions. These QTL will facilitate the understanding of the genetic basis as well as facilitate breeding cultivars for drought and salt tolerance through marker-assisted selection (MAS). Since 1994 when the first linkage map was constructed in cotton (AJ et al., 1994) from an interspecific cross between Pima and Upland cotton using 705 loci of restricted fragment polymorphic markers (RFLPs), numerous linkage maps have been constructed to dissect different complex traits in cotton using different types of markers. However, most of these linkage maps have been used to identify QTL for yield and its component traits and fiber quality under normal production conditions, and only a few studies have been conducted to identify QTL for traits related to abiotic stress tolerance. As stated above, there are many traits related to abiotic stress tolerance in cotton such as leaf shape and morphology, biomass traits, and physiological traits that all contribute to the final production of lint yield. For example, as the studies with the Okra-leaf cotton type showed, leaf architecture can improve drought tolerance by affecting early maturity, reducing leaf area index, and increasing photosynthesis (Pettigrew et al., 1993). Jiang et al. (2000) used 180 F2 plants from an interspecific hybrid between Upland and a wild type G. barbadense and mapped 40 QTL related to leaf morphology using 261 polymorphic RFLPs. The largest QTL cluster was found on chromosome c15, corresponding to the Okra-leaf locus. They also mapped a locus on chromosome c6 that affects trichrome density on leaves, which plays a critical role under drought stress by affecting the transpiration rate. This finding along with results by Wright et al. (1999) using different cotton population types also based on RFLPs, indicates that genetic variation in trichrome exists in cotton. (Saranga et al. (2001, 2004) used early segregating populations from an interspecific cross between G. hirsutum and G. barbadense to detect QTL that were associated with water stress tolerance based on 253 RFLPs. Many different traits were studied including, physiological traits: osmotic potential, carbon isotope ratio (13C), canopy temperature, and chlorophyll a and b content; traits related to yield: dry matter, 124

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and biotic stress resistance QTL for physiological responses, yield and its components traits, as well as fiber quality traits measured under abioitc and biotic stress conditions. The distribution of tolerance QTL are not uniform across the cotton genome, as 23 QTL clusters were identified on 15 different chromosomes (c3, c4, c5, c6, c7, c11, c14, c15, c16, c19, c20, c23, c24, c25, and c26) for stress tolerance. Furthermore, 28 QTL hotspots were identified for different stress tolerance traits. Most importantly, two QTL hotspots were identified on chromosome c24 for chlorophyll content measured under drought and salt tolerance using a SPAD meter. This meta-analysis will be frequently updated by adding newly reported QTL in cotton.

example, a RIL population of 146 lines was evaluated in the greenhouse for osmotic stress tolerance using PEG by Abdelraheem et al. (2015a), for salt stress by Tiwari (Tiwari et al., 2013b), and for drought tolerance under the field conditions by (Adams et al., 2011). An important finding was that the marker interval between two sequence tagged site (STS) markers (IH200-STS- IH590-STS) was associated with shoot weight under PEG stress in the greenhouse and with seedcotton yield, lint yield, fiber strength, and fiber uniformity under drought stress conditions in the field. The marker interval between two SSR markers (MUSS096-MUSS009) was associated with fresh shoot weight under PEG stress and lint percent under field conditions. Marker interval 1F470-1F480 was associated with plant height under both PEG and NaCl stresses in the greenhouse and fiber strength under field conditions. Interestingly, our previous studies reported that Upland parents also carry desirable QTL alleles responsible for salt and drought tolerance in the same BIL population (Tiwari et al., 2013b; Adams et al., 2011). These findings, along with the correlation between osmotic adjustment and seedcotton yield as reported by Saranga et al. (2004) indicate that favorable alleles for abiotic and biotic stress resistance in cotton can originate from either sensitive G. hirsutum or tolerant G. barbadense, thus recombination of favorable alleles from each of these species will help in discovering complementary allele combinations across the polyploidy cotton genome. The genome-wide association study (GWAS) in crops including cotton uses much broader genotypes and inexpensive genome-wide DNA markers (Zhu et al., 2008) for whole genome coverage. This technology gives a higher statistical power to detect major QTL with a high resolution that can explain more phenotypic variation than a biparental mapping population. In cotton, a few studies have been conducted under abiotic stress conditions. Although such studies had a large number of genotypes, most of them only used low genome coverage of SSR markers. Jia et al. (2014) evaluated 323 Upland accessions for drought and salt tolerance and performed GWAS using 106 SSR markers. Drought tolerance was associated with 15 SSR markers and salt tolerance with three SSR markers, and there was no overlap between the two classes of stress markers. Du et al. (2017) also performed GWAS in 304 Upland accessions for salt tolerance using 145 SSR markers. A total of 95 loci were significantly associated with salt tolerance traits. SNPs with their broad genome-wide distribution are excellent candidates for GWAS to link phenotypes to genotypes. Abdelraheem (2017a) evaluated a total of 376 Upland cotton accessions in the greenhouse for abiotic and biotic stress tolerances in replicated tests and performed GWAS using 26,301 polymorphic SNPs from the CottonSNP63 K array to identify abiotic stress tolerance QTL. Major shared QTL were detected for abiotic and biotic stress tolerances, indicating that these QTL may share similar genetic components. Based on dry shoot and root weights, main-effect QTL were detected for drought on chromosomes c8, c15, c21, c24, c25, and c26, and for salt tolerance on c1, c9, c11, c12, c13, c14, c18, c21, and c24. Abdelraheem et al. (2018b) also confirmed these results by performing GWAS in a MAGIC population of Upland cotton consisting of 550 recombinant inbred lines using more than 470,000 SNPs based on the reference genome sequence from TM-1. A total of 27 and 16 QTL were detected based on plant height and dry shoot weight, respectively, under both drought and salt stress conditions. Eleven QTL were identified to be common between drought and salt tolerance. As more QTL are reported from different studies, meta-analyses can be performed using markers shared across the studies to identify common QTL across tests. Said et al. (2013) conducted the first comprehensive QTL meta-analysis in cotton by compiling a total of 1223 QTL for yield, fiber quality, disease resistance and drought tolerance. However, no QTL cluster and/or QTL hotspots were detected for drought tolerance due to the low number of drought tolerance QTL reported. Recently, Abdelraheem et al. (2017b) conducted a follow-up meta-analysis to identify QTL clusters and hotspots among 661 abiotic

8. Transgenic approaches to improve drought and salt tolerance in cotton Transgenic technology is an important approach that has been employed toward improving plant abiotic tolerance by creating stressresistant plants. Many studies were conducted to explore the response of plants at the molecular level to drought and salt stresses, which resulted in discovering a wide range of stress-related genes (Farooq et al., 2009). Studying the stress-related genes is of great interest for scientists, as they can use the knowledge in improving plant’s stress tolerance through transgenic approaches (Shinozaki and YamaguchiShinozaki, 2007). Transcription factors play a critical role in plant response to abioitc stress. For instance, when GhABF2, a bZIP transcription factor gene, was overexpressed in cotton, the transgenic plants demonstrated drought and salt tolerance via regulation of ABA-related genes. GhABF2-overexpressing cotton plants also displayed an improved yield compared to non-transgenic control plants (Liang et al., 2016b). Mittal et al. (2014) overexpressed AtRAV1/2, a basic 3-DNAbinding domain transcription factor gene, and AtABI5, a basic leucine zipper transcription factor gene, in cotton and observed an improved drought tolerant phenotype. The rice SNAC1, a member of the NAC family of transcription factors gene, was overexpressed in cotton by (Liu et al., 2014). The SNAC1-overexpressing cotton plants are more drought and salt tolerant and they produced a more robust rooting system with reduced transpiration rate compared to non-transgenic cotton plants (Liu et al., 2014; Yu et al., 2016) overexpressed the Arabidopsis ENHANCED DROUGHT TOLERANCE1/HOMEODOMAIN GLABROUS11 (AtEDT1/HDG11) gene in cotton, and these transgenic cotton plants demonstrated an improved drought and salt tolerance. A larger rooting system, higher proline content in leaves, and a significantly higher activity of ROS scavenging enzymes were observed in AtEDT1/HDG11 overexpressing cotton Yu et al. (2016). There are several studies demonstrating improved drought and/or salt tolerance in transgenic cotton carrying overexpressed stress-related genes important in cell physiology (Ullah et al., 2017). For instance, overexpression of TsVP, a H+-PPase gene from Thellungiella halophile, improved drought tolerance in cotton with higher photosynthetic rates compared to non-transgenic plants (Lv et al., 2009). Transgenic cotton with this H+-PPase, also had enhanced salt tolerance and improved cotton growth under salt stress conditions (Lv et al., 2008). An improved drought and salt tolerance was achieved in transgenic cotton plants overexpressing the Arabidopsis vacuolar H+-pyrophosphatase gene, AVP1, and transgenic plants produced higher yield compared to non-transgenic plants under stress conditions (Pasapula et al., 2011). The overexpression of Arabidopsis vacuolar Na+/H+antiporter gene AtNHX1 in cotton also resulted in an improved drought and salt tolerance in greenhouse and field conditions and higher fiber yield was produced compared to non-transgenic cotton (Umezawa et al., 2006). Moreover, Shen et al. (2015) co-overexpressed AVP1 and AtNHX1 genes in cotton, and showed an improved salt and drought tolerance in AVP1/ AtNHX1 co-overexpressing cotton plants compared to non-transgenic plants. Transgenic cotton co-overexpressing AVP1 and AtNHX1produced 24% and 35% more fiber than non-transgenic plants under lowirrigation and dryland conditions, respectively (Shen et al., 2015). 125

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transgenic approaches. Many genes that are commonly associated with plant drought or salt tolerance have been introduced to cotton for enhancement of abiotic stress tolerance through genetic engineering. However, it should be pointed out that, none of the genes have been utilized in commercial cotton breeding programs. Promising drought or salt tolerance genes are often observed to have other undesirable effects on cotton growth through gene-silencing or overexpression approaches due to the interconnectedness between drought/salt response and many other aspects of plant growth. An efficient approach is likely dependent on the utilization of natural variation in multiple drought or salt tolerance genes or alleles in cotton, although no abiotic stress tolerance QTL has been currently used in cotton breeding through marker-assisted selection (MAS). It is expected that more and large permanent intra-specific and interspecific linkage mapping populations using diverse and multiple parents will be developed for repeated phenotyping for abiotic stress tolerance and for high resolution mapping of QTL using genome-wide SNP markers. Large effect stress tolerance QTL with anchored markers will be identified for MAS to transfer tolerance genes to high-yielding cultivars. In addition, quick, reliable and high throughput screening methods applicable on a large scale should be developed to improve the reliability and scale of phenotyping cotton germplasm for drought and salt stress tolerance.

(Kuppu et al., 2013) overexpressed the isopentenyltransferase gene (IPT), which is involved in cytokinin biosynthesis, to enhance drought tolerance. Further physiological studies on IPT-overexpressing cotton plants showed that the yield of transgenic cotton is strongly dependent on the timing of the drought stress. A study by (Zhu et al., 2018), illustrated that, IPT-transgenic cotton outperforms the non-transgenic cotton only if the drought stress occurs before the flowering stage. Similar results were shown by (Liu et al., 2012). They demonstrated that overexpression of IPT in cotton improves salt tolerance, delays leaf senescence, and increases plant biomass in transgenic cotton compared to non-transgenic cotton plants (Liu et al., 2012). Recently, (Mishra et al., 2017) demonstrated that overexpression in cotton of the SUMO E3 ligase gene from rice, OsSIZ1, improved stress tolerance to heat and drought, and significantly increased fiber yield in a dryland agricultural system. GHSP2 is a small heat shock protein in G. arboreum L. which is also induced by drought. Overexpression of GHSP2 improves drought stress tolerance in G. hirsutum (Maqbool et al., 2010). LOS5/ABA3 encodes a molybdenum binding co-factor and is required for proper functioning of the aldehyde oxidase involved in ABA biosynthesis. Transgenic cotton overexpressing the Arabidopsis gene AtLOS5 led to increased ABA levels, which in turn led to an improved drought tolerance. Transgenic plants produced approximately 13% more fresh biomass compared to non-transgenic cotton (Yue et al., 2012). Recently, Zhang et al. (2015) reported an improved drought tolerance achieved by overexpression of GhAnn1 that encodes a higher activity of SOD in cotton plants. In a study by (Chen et al., 2015), downregulation of GbMYb5 led to a higher rate of oxidative stress under drought conditions due to a reduction in activities of POD, SOD, and CAT enzymes. Arabidopsis GF14 < lambda > that encodes the 14-3-3 protein was overexpressed in cotton plants. GF14 λ-overxpressing cotton exhibited an improved drought tolerance and maintained higher photosynthetic rates under water deprivation conditions (Yan et al., 2004). Choline monooxygenase (CMO) is involved in the synthesis of glycine betaine. In a study by (Zhang et al., 2010), the CMO gene from Atriplexhortensis was overexpressed in cotton, which resulted in improved salinity tolerance. The transgenic approach appears to be a powerful and impactful method to improve crop tolerance to abiotic stresses including salinity and water deprivation.

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9. Perspective and concluding remarks The mechanisms in cotton to display tolerance to different abiotic stresses appear interconnected and may have overlapping genetic elements. However, the genetic bases for these tolerances are not fully understood due to the complexity of the stress conditions and difficulties in phenotyping, which are influenced by multiple genes with small and varying effects and environmental factors. Both drought and salt stresses negatively affect molecular, biochemical and physiological processes, which eventually leads to suppressed growth and development in cotton, including decreased photosynthetic rate, plant height, leaf and root size, biomass, and economic yield, yield components, and poorer fiber quality. Therefore, multiple traits such as these mentioned above can be used to screen cotton for drought and salt tolerance grown in field (yield, yield components and fiber quality) or greenhouse (plant height and biomass) conditions. However, reliably evaluating cotton for abiotic stress tolerance is difficult, and heritability estimates of many abiotic stress tolerance related traits particularly physiological traits and yield traits are low. Furthermore, linkage drag between genes for desirable and undesirable traits is still a big challenge to improve cotton for abiotic stress tolerance through direct selections due to the negative correlation between yield and abiotic stress tolerance. However, significant progress has been made in understanding the genetic basis of drought and salt tolerance through QTL mapping using molecular markers on biparental and multi-parental populations and natural populations. In the last 10–15 years, numerous drought or salt responsive genes have been identified, some of which were further studied using 126

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