Rice Curled Its Leaves Either Adaxially or Abaxially to Combat Drought Stress

doi:10.1016/j.rsci.2023.04.002

Abstract

Abstract:

Leaf rolling (LR) is one of the defensive mechanisms that plants have developed against adverse environmental conditions. LR is a typical drought response, promoting drought resistance in various gramineae species, including wheat, maize, and rice. Rice cultivation faces the formidable challenge of water deprivation because of its high water requirements, which leads to drought-related symptoms in rice. LR is an important morphological characteristic that plays a key role in controlling water loss during water insufficiency, thereby regulating leaf area and stature, which are crucial agronomic traits determining yield criteria. Bulliform, sclerenchyma, mesophyll, and vascular bundles are the cells that engage in LR and commonly exhibit adaxial or abaxial types of rolling in rice. The specific genes linked to rolling, either adaxially or abaxially, are discussed here. In addition to the factors influencing LR, here is a short review of the morphological, physiological and molecular responses of this adaptation under drought stress. Moreover, this review highlights how LR combats the consequences of drought stress. The eco-physiological and molecular mechanisms underlying this morphological adaptation in rice should be further explored, as they might be useful in dealing with various degrees of drought tolerance.

Key words: adaxial/abaxial rolling, drought stress, leaf rolling, molecular mechanism, rice, physiological response, transcript factor

Ammara Latif, Sun Ying, Pu Cuixia, Noman Ali. Rice Curled Its Leaves Either Adaxially or Abaxially to Combat Drought Stress[J]. Rice Science, 2023, 30(5): 405-416.

Figures/Tables 8

References 103

[1]	Ahmad M S A, Javed F, Ashraf M. 2007. Iso-osmotic effect of NaCl and PEG on growth, cations and free proline accumulation in callus tissue of two indica rice (Oryza sativa L.) genotypes. Plant Growth Regul, 53(1): 53-63.
[2]	Amal B A, Said M, Abdelaziz B, Mouhammed M, Nasser E N,Bouhmadi Keltoum E. 2020. Relationship between leaf rolling and some physiological parameters in durum wheat under water stress. Afr J Agric Res, 16(7): 1061-1068.
[3]	Anjum S A, Xie X Y, Wang L C, Saleem M F, Man C, Lei W. 2011. Morphological, physiological and biochemical responses of plants to drought stress. Afr J Agric Res, 6(9): 2026-2032.
[4]	Baret F, Madec S, Irfan K, Lopez J, Comar A, Hemmerlé M, Dutartre D, Praud S, Tixier M H. 2018. Leaf-rolling in maize crops: From leaf scoring to canopy-level measurements for phenotyping. J Exp Bot, 69(10): 2705-2716. PMID
[5]	Barik S R, Pandit E, Pradhan S K, Mohanty S P, Mohapatra T. 2019. Genetic mapping of morpho-physiological traits involved during reproductive stage drought tolerance in rice. PLoS One, 14(12): e0214979.
[6]	Bharteey P K, Singh Y V, Deka B, Dutta M. 2020. Assessment of water requirement for major crops of Mirzapur district in eastern Uttar Pradesh. Ann Plant Res Soil, 22(1): 100-106.
[7]	Bouman B A M, Lampayan R M, Tuong T P. 2007. Water Management in Irrigated Rice: Coping with Water Scarcity. Los Banos, the Philippines: International Rice Research Institute.
[8]	Cal A J, Sanciangco M, Rebolledo M C, Luquet D, Torres R O, McNally K L, Henry A. 2019. Leaf morphology, rather than plant water status, underlies genetic variation of rice leaf rolling under drought. Plant Cell Environ, 42(5): 1532-1544.
[9]	Canales C, Grigg S, Tsiantis M. 2005. The formation and patterning of leaves: Recent advances. Planta, 221(6): 752-756. PMID
[10]	Chaves M M, Flexas J, Pinheiro C. 2009. Photosynthesis under drought and salt stress: Regulation mechanisms from whole plant to cell. Ann Bot, 103(4): 551-560.
[11]	Chen F, Aqeel M, Khalid N, Irshad M K, Farhat F, Nazir A, Ma J, Akhtar M S, Eldesoky G E, Aljuwayid A M, Noman A. 2023. Glutathione treatment suppresses the adverse effects of microplastics in rice. Chemosphere, 322: 138079.
[12]	Chen Q L, Xie Q J, Gao J, Wang W Y, Sun B, Liu B H, Zhu H T, Peng H F, Zhao H B, Liu C H, Wang J, Zhang J L, Zhang G Q, Zhang Z M. 2015. Characterization of Rolled and Erect Leaf 1 in regulating leave morphology in rice. J Exp Bot, 66(19): 6047-6058.
[13]	Cho S H, Lee C H, Gi E, Yim Y, Koh H J, Kang K, Paek N C. 2018. The rice rolled fine striped (RFS) CHD3/Mi-2 chromatin remodeling factor epigenetically regulates genes involved in oxidative stress responses during leaf development. Front Plant Sci, 9: 364.
[14]	Choi S Y, Lee Y J, Seo H U, Kim J H, Jang C S. 2022. Physio- biochemical and molecular characterization of a rice drought- insensitive TILLING line 1 (ditl1) mutant. Physiol Plant, 174(3): e13718.
[15]	Crang R, Lyons-Sobaski S, Wise R. 2018. Plant Anatomy: A Concept-Based Approach to the Structure of Seed Plants. Springer Nature Swetzerland AG: Springer: 181-213.
[16]	De Rybel B, Mähönen A P, Helariutta Y, Weijers D. 2016. Plant vascular development: From early specification to differentiation. Nat Rev Mol Cell Biol, 17(1): 30-40.
[17]	Dharminder C, Singh R K, Kumar V, Devedee A K, Mruthyunjaya M, Reshu B. 2019. The clean water: The basic need of human and agriculture. Int J Chem Stud, 7(2): 1994-1998.
[18]	Fang J J, Guo T T, Xie Z W, Chun Y, Zhao J F, Peng L X, Zafar S A, Yuan S J, Xiao L T, Li X Y. 2021. The URL1-ROC5-TPL2 transcriptional repressor complex represses the ACL1 gene to modulate leaf rolling in rice. Plant Physiol, 185(4): 1722-1744.
[19]	Fang L K, Zhao F M, Cong Y F, Sang X C, Du Q, Wang D Z, Li Y F, Ling Y H, Yang Z L, He G H. 2012. Rolling-leaf14 is a 2OG-Fe (II) oxygenase family protein that modulates rice leaf rolling by affecting secondary cell wall formation in leaves. Plant Biotechnol J, 10(5): 524-532. PMID
[20]	Fang Y J, Xiong L Z. 2015. General mechanisms of drought response and their application in drought resistance improvement in plants. Cell Mol Life Sci, 72(4): 673-689. PMID
[21]	Farooq M, Wahid A, Kobayashi N, Fujita D, Basra S M A. 2009. Plant drought stress: Effects, mechanisms and management. Agron Sustain Dev, 29: 185-212.
[22]	Fischer T R, Byerlee D, Edmeades G O. 2009. Can technology deliver on the yield challenge to 2050? In: Conforti P. Looking Ahead in World Food and Agriculture: Perspectives to 2050 FAO: Agricultural Development Economics Division Economic and Social Development Department.
[23]	Fujino K, Matsuda Y, Ozawa K, Nishimura T, Koshiba T, Fraaije M W, Sekiguchi H. 2008. NARROW LEAF 7 controls leaf shape mediated by auxin in rice. Mol Genet Genomics, 279(5): 499-507. PMID
[24]	Guo T T, Wang D F, Fang J J, Zhao J F, Yuan S J, Xiao L T, Li X Y. 2019. Mutations in the rice OsCHR4 gene, encoding a CHD3 family chromatin remodeler, induce narrow and rolled leaves with increased cuticular wax. Int J Mol Sci, 20(10): 2567.
[25]	Hellal F A, El-Shabrawi H M, Abd El-Hady M, Khatab I A, El-Sayed S A, Abdelly C. 2018. Influence of PEG induced drought stress on molecular and biochemical constituents and seedling growth of Egyptian barley cultivars. J Genet Eng Biotechnol, 16(1): 203-212. PMID
[26]	Hibara K I, Obara M, Hayashida E, Abe M, Ishimaru T, Satoh H, Itoh J I, Nagato Y. 2009. The ADAXIALIZED LEAF1gene functions in leaf and embryonic pattern formation in rice. Dev Biol, 334(2): 345-354.
[27]	Hsiao T C, O’Toole J C, Yambao E B, Turner N C. 1984. Influence of osmotic adjustment on leaf rolling and tissue death in rice (Oryza sativa L.). Plant Physiol, 75(2): 338-341. PMID
[28]	Hu J, Zhu L, Zeng D L, Gao Z Y, Guo L B, Fang Y X, Zhang G H, Dong G J, Yan M X, Liu J, Qian Q. 2010. Identification and characterization of NARROW AND ROLLED LEAF 1, a novel gene regulating leaf morphology and plant architecture in rice. Plant Mol Biol, 73(3): 283-292.
[29]	Huang J, Li Z Y, Zhao D Z. 2016. Deregulation of the OsmiR160 target gene OsARF18 causes growth and developmental defects with an alteration of auxin signaling in rice. Sci Rep, 6: 29938. PMID
[30]	Irshad M K, Ibrahim M, Noman A, Shang J Y, Mahmood A, Mubashir M, Khoo K S, Ng H S, Show P L. 2022. Elucidating the impact of goethite-modified biochar on arsenic mobility, bioaccumulation in paddy rice (Oryza sativa L.) along with soil enzyme activities. Process Saf Environ Prot, 160: 958-967.
[31]	Islam M M, Kayesh E, Zaman E, Urmi T A, Haque M M. 2018. Evaluation of rice (Oryza sativa L.) genotypes for drought tolerance at germination and early seedling stage. Agriculturists, 16(1): 44-54.
[32]	Itoh J I, Nonomura K I, Ikeda K, Yamaki S, Inukai Y, Yamagishi H, Kitano H, Nagato Y. 2005. Rice plant development: From zygote to spikelet. Plant Cell Physiol, 46(1): 23-47.
[33]	Juarez M T, Twigg R W, Timmermans M C. 2004. Specification of adaxial cell fate during maize leaf development. Development, 131(18): 4533-4544. PMID
[34]	Kadioglu A, Terzi R. 2007. A dehydration avoidance mechanism: Leaf rolling. Bot Rev, 73(4): 290-302.
[35]	Kadioglu A, Saruhan N, Sağlam A, Terzi R, Acet T. 2011. Exogenous salicylic acid alleviates effects of long term drought stress and delays leaf rolling by inducing antioxidant system. Plant Growth Regul, 64(1): 27-37.
[36]	Kadioglu A, Terzi R, Saruhan N, Saglam A. 2012. Current advances in the investigation of leaf rolling caused by biotic and abiotic stress factors. Plant Sci, 182: 42-48. PMID
[37]	Kahlown M A, Kemper W D. 2007. Factors affecting success and failure of trickle irrigation systems in Balochistan, Pakistan. Irrig Sci, 26(1): 71-79.
[38]	Khew C Y, Teo C J, Chan W S, Wong H L, Namasivayam P, Ho C L. 2015. Brassinosteroid insensitive 1-associated kinase 1 (OsI- BAK1) is associated with grain filling and leaf development in rice. J Plant Physiol, 182: 23-32.
[39]	Lafitte H R, Blum A, Atlin G. 2003. Using secondary traits to help identify drought-tolerant genotypes. In: Fischer K S, Lafitte R, Fukai S, Atlin G, Hardy B. Breeding Rice for Drought-Prone Environments, the Philippines: International Rice Research Institute: 37-48.
[40]	Lang Y Z, Zhang Z J, Gu X Y, Yang J C, Zhu Q S. 2004. Physiological and ecological effects of crimpy leaf character in rice (Oryza sativa L.): II. Acta Agron Sin, 30(9): 883-887. (in Chinese with English abstract)
[41]	Li C, Zou X H, Zhang C Y, Shao Q H, Liu J, Liu B, Li H Y, Zhao T. 2016. OsLBD3-7 overexpression induced adaxially rolled leaves in rice. PLoS One, 11(6): e0156413.
[42]	Li L, Shi Z Y, Li L, Shen G Z, Wang X Q, An L S, Zhang J L. 2010. Overexpression of ACL1 (abaxially curled leaf 1) increased bulliform cells and induced abaxial curling of leaf blades in rice. Mol Plant, 3(5): 807-817.
[43]	Li M, Li X Z, Zhu L, Xue P B, Bao J L, Zhou B B, Jin J, Wang J. 2022. Genome-wide transcriptomic analysis reveals the gene regulatory network controlled by SRL1 in regulating rice leaf rolling. J Plant Growth Regul, 41(6): 2292-2304.
[44]	Li S X, Wang Z H, Malhi S S, Li S Q, Gao Y J, Tian X H. 2009. Chapter 7: Nutrient and water management effects on crop production, and nutrient and water use efficiency in dryland areas of China. Adv Agron, 102: 223-265.
[45]	Li W Q, Zhang M J, Gan P F, Qiao L, Yang S Q, Miao H, Wang G F, Zhang M M, Liu W T, Li H F, Shi C H, Chen K M. 2017. CLD1/SRL1 modulates leaf rolling by affecting cell wall formation, epidermis integrity and water homeostasis in rice. Plant J, 92(5): 904-923.
[46]	Liu F, Wang P D, Zhang X B, Li X F, Yan X H, Fu D H, Wu G. 2018. The genetic and molecular basis of crop height based on a rice model. Planta, 247(1): 1-26. PMID
[47]	Ma J, Aqeel M, Khalid N, Nazir A, Alzuaibr F M, Al-Mushhin A A M, Hakami O, Iqbal M F, Chen F, Alamri S, Hashem M, Noman A. 2022. Effects of microplastics on growth and metabolism of rice (Oryza sativa L.). Chemosphere, 307: 135749.
[48]	Ma Y H, Zhao Y, Shangguan X X, Shi S J, Zeng Y, Wu Y, Chen R Z, You A Q, Zhu L L, Du B, He G C. 2017. Overexpression of OsRRK1 changes leaf morphology and defense to insect in rice. Front Plant Sci, 8: 1783.
[49]	Maclean J L, Dawe D C, Hardy B, Hettel G P. 2002. Rice Almanac: Source Book for the Most Important Economic Activity on Earth. Wallingford: CABI.
[50]	Mahmood T, Abdullah M, Ahmar S, Yasir M, Iqbal M S, Yasir M, Ur Rehman S, Ahmed S, Rana R M, Ghafoor A, Nawaz Shah M K, Du X M, Mora-Poblete F. 2020. Incredible role of osmotic adjustment in grain yield sustainability under water scarcity conditions in wheat (Triticum aestivum L.). Plants, 9(9): 1208.
[51]	Mangena P. 2018. Water stress: Morphological and anatomical changes in soybean (Glycine max L.) plants. In: Andjelkovic V. Plant, Abiotic Stress and Responses to Climate Change. IntechOpen: 9-31.
[52]	Matschi S, Vasquez M F, Bourgault R, Steinbach P, Chamness J, Kaczmar N, Gore M A, Molina I, Smith L G. 2020. Structure- function analysis of the maize bulliform cell cuticle and its potential role in dehydration and leaf rolling. Plant Direct, 4(10): e00282.
[53]	Matsumoto H, Yasui Y, Kumamaru T, Hirano H Y. 2018. Characterization of a half-pipe-like leaf1 mutant that exhibits a curled leaf phenotype. Genes Genet Syst, 92(6): 287-291. PMID
[54]	Matsumoto H, Yasui Y, Ohmori Y, Tanaka W, Ishikawa T, Numa H, Shirasawa K, Taniguchi Y, Tanaka J, Suzuki Y, Hirano H Y. 2020. CURLED LATER1 encoding the largest subunit of the Elongator complex has a unique role in leaf development and meristem function in rice. Plant J, 104(2): 351-364.
[55]	Nar H, Saglam A, Terzi R, Várkonyi Z, Kadioglu A. 2009. Leaf rolling and photosystem II efficiency in Ctenanthe setosa exposed to drought stress. Photosynthetica, 47(3): 429-436.
[56]	Nikolaeva M K, Maevskaya S N, Shugaev A G, Bukhov N G. 2010. Effect of drought on chlorophyll content and antioxidant enzyme activities in leaves of three wheat cultivars varying in productivity. Russ J Plant Physiol, 57(1): 87-95.
[57]	Osakabe Y, Osakabe K, Shinozaki K, Tran L S P. 2014. Response of plants to water stress. Front Plant Sci, 5: 86. PMID
[58]	Pina A L C B, Zandavalli R B, Oliveira R S, Martins F R, Soares A A. 2016. Dew absorption by the leaf trichomes of Combretum leprosum in the Brazilian semiarid region. Funct Plant Biol, 43(9): 851-861. PMID
[59]	Praharaj C S, Singh U, Singh S S, Singh N P, Shivay Y S. 2016. Supplementary and life-saving irrigation for enhancing pulses production, productivity and water-use efficiency in India. Ind J Agron, 61: S249-S261.
[60]	Rahaman M M, Shehab M K. 2018. Is the propensity of increasing the rice production a sustainable approach? Experiences from India, Pakistan, and Bangladesh. J Water Resour Eng Manag, 5(2): 12-28.
[61]	Rahman H, Ramanathan V, Nallathambi J, Duraialagaraja S, Muthurajan R. 2016. Over-expression of a NAC 67 transcription factor from finger millet (Eleusine coracana L.) confers tolerance against salinity and drought stress in rice. BMC Biotechnol, 16(Suppl 1): 35.
[62]	Rodriguez R E, Debernardi J M, Palatnik J F. 2014. Morphogenesis of simple leaves: Regulation of leaf size and shape. Wiley Interdiscip Rev Dev Biol, 3(1): 41-57.
[63]	Rontein D, Dieuaide-Noubhani M, Dufourc E J, Raymond P, Rolin D. 2002. The metabolic architecture of plant cells: Stability of central metabolism and flexibility of anabolic pathways during the growth cycle of tomato cells. J Biol Chem, 277(46): 43948-43960. PMID
[64]	Saijo Y, Hata S, Kyozuka J, Shimamoto K, Izui K. 2000. Over- expression of a single Ca²⁺-dependent protein kinase confers both cold and salt/drought tolerance on rice plants. Plant J, 23(3): 319-327. PMID
[65]	Sakurai N, Katayama Y, Yamaya T. 2001. Overlapping expression of cytosolic glutamine synthetase and phenylalanine ammonia- lyase in immature leaf blades of rice. Physiol Plant, 113(3): 400-408. PMID
[66]	Salehi-Lisar S Y, Bakhshayeshan-Agdam H. 2016. Drought stress in plants:Causes, consequences, and tolerance. In: Hossain M A, Wani S H, Bhattacharjee S, Burritt D J, Tran L P. Drought Stress Tolerance in Plants:Vol. 1. Physiology and Biochemistry. Spring Nature Swetzerland AG: Springer Cham.
[67]	Sarkar S, Islam A K M A, Barma N C D, Ahmed J U. 2021. Tolerance mechanisms for breeding wheat against heat stress: A review. S Afr J Bot, 138: 262-277.
[68]	Seleiman M F, Al-Suhaibani N, Ali N, Akmal M, Alotaibi M, Refay Y, Dindaroglu T, Abdul-Wajid H H, Battaglia M L. 2021. Drought stress impacts on plants and different approaches to alleviate its adverse effects. Plants, 10(2): 259.
[69]	Singh B, Reddy K R, Diaz Redoña E, Walker T. 2017. Screening of rice cultivars for morpho-physiological responses to early- season soil moisture stress. Rice Sci, 24(6): 322-335.
[70]	Singh S, Koyama H, Bhati K K, Alok A. 2021. The biotechnological importance of the plant-specific NAC transcription factor family in crop improvement. J Plant Res, 134: 475-495. PMID
[71]	Subashri M, Robin S, Vinod K K, Rajeswari S, Mohanasundaram K, Raveendran T S. 2009. Trait identification and QTL validation for reproductive stage drought resistance in rice using selective genotyping of near flowering RILs. Euphytica, 166(2): 291-305.
[72]	Sun J, Cui X A, Teng S Z, Zhao K N, Wang Y W, Chen Z H, Sun X H, Wu J X, Ai P F, Quick W P, Lu T G, Zhang Z G. 2020. HD-ZIP IV gene Roc8 regulates the size of bulliform cells and lignin content in rice. Plant Biotechnol J, 18(12): 2559-2572.
[73]	Tee E E. 2020. Journey and destination: KORRIGAN1 subcellular localization dynamically changes during plant growth and stress tolerance. Plant Cell, 32(2): 291-292.
[74]	Ullah H, Santiago-Arenas R, Ferdous Z, Attia A, Datta A. 2019. Improving water use efficiency, nitrogen use efficiency, and radiation use efficiency in field crops under drought stress: A review. Adv Agron, 156: 109-157.
[75]	Upadhyaya A. 2019. Multi-objective fuzzy linear programming for land allocation under different crops in bhagwanpur distributary. J AgriSearch, 6(4): 188-193.
[76]	Valliyodan B, Nguyen H T. 2006. Understanding regulatory networks and engineering for enhanced drought tolerance in plants. Curr Opin Plant Biol, 9(2): 189-195. PMID
[77]	Venuprasad R, Bool M E, Quiatchon L, Sta Cruz M T, Amante M, Atlin G N. 2012. A large-effect QTL for rice grain yield under upland drought stress on chromosome 1. Mol Breed, 30(1): 535-547.
[78]	Wang L, Xu J, Nian J Q, Shen N W, Lai K K, Hu J, Zeng D L, Ge C W, Fang Y X, Zhu L, Qian Q, Zhang G H. 2016. Characterization and fine mapping of the rice gene OsARVL4 regulating leaf morphology and leaf vein development. Plant Growth Regul, 78(3): 345-356.
[79]	Wu R H, Li S B, He S, Wassmann F, Yu C H, Qin G J, Schreiber L, Qu L J, Gu H Y. 2011. CFL1, a WW domain protein, regulates cuticle development by modulating the function of HDG1, a class IV homeodomain transcription factor, in rice and Arabidopsis Plant Cell, 23(9): 3392-3411.
[80]	Xiang J J, Zhang G H, Qian Q, Xue H W. 2012. SEMI-ROLLED LEAF1 encodes a putative glycosylphosphatidylinositol-anchored protein and modulates rice leaf rolling by regulating the formation of bulliform cells. Plant Physiol, 159(4): 1488-1500.
[81]	Xu P Z, Ali A, Han B L, Wu X J. 2018. Current advances in molecular basis and mechanisms regulating leaf morphology in rice. Front Plant Sci, 9: 1528. PMID
[82]	Xu Y, Wang Y H, Long Q Z, Huang J X, Wang Y L, Zhou K N, Zheng M, Sun J, Chen H, Chen S H, Jiang L, Wang C M, Wan J M. 2014. Overexpression of OsZHD1, a zinc finger homeodomain class homeobox transcription factor, induces abaxially curled and drooping leaf in rice. Planta, 239(4): 803-816.
[83]	Xu Y, Kong W Y, Wang F Q, Wang J, Tao Y J, Li W Q, Chen Z H, Fan F J, Jiang Y J, Zhu Q H, Yang J. 2021. Heterodimer formed by ROC8 and ROC5 modulates leaf rolling in rice. Plant Biotechnol J, 19(12): 2662-2672. PMID
[84]	Xue D W, Zhang X Q, Lu X L, Chen G, Chen Z H. 2017. Molecular and evolutionary mechanisms of cuticular wax for plant drought tolerance. Front Plant Sci, 8: 621. PMID
[85]	Yang S Q, Li W Q, Miao H, Gan P F, Qiao L, Chang Y L, Shi C H, Chen K M. 2016. REL2, a gene encoding an unknown function protein which contains DUF630 and DUF632 domains controls leaf rolling in rice. Rice, 9(1): 37.
[86]	Young T E, Meeley R B, Gallie D R. 2004. ACC synthase expression regulates leaf performance and drought tolerance in maize. Plant J, 40(5): 813-825. PMID
[87]	Yu N, Liang Y P, Wang Q P, Peng X X, He Z H, Hou X W. 2022. Transcriptomic analysis of OsRUS1 overexpression rice lines with rapid and dynamic leaf rolling morphology. Sci Rep, 12(1): 6736.
[88]	Yu S, Tian L. 2018. Breeding major cereal grains through the lens of nutrition sensitivity. Mol Plant, 11(1): 23-30. PMID
[89]	Yu X Q, Xie W, Liu H, Liu W, Zeng D L, Qian Q, Ren D Y. 2022. Characterization and fine mapping of a semi-rolled leaf mutant srl3 in rice. J Integr Agric, 21(11): 3103-3113.
[90]	Yuan S, Li Y, Peng S B. 2015. Leaf lateral asymmetry in morphological and physiological traits of rice plant. PLoS One, 10(6): e0129832.
[91]	Zhang G H, Xu Q, Zhu X D, Qian Q, Xue H W. 2009. SHALLOT- LIKE1 is a KANADI transcription factor that modulates rice leaf rolling by regulating leaf abaxial cell development. Plant Cell, 21(3): 719-735.
[92]	Zhang G H, Hou X, Wang L, Xu J, Chen J, Fu X, Shen N W, Nian J Q, Jiang Z Z, Hu J, Zhu L, Rao Y C, Shi Y F, Ren D Y, Dong G J, Gao Z Y, Guo L B, Qian Q, Luan S. 2021. PHOTO- SENSITIVE LEAF ROLLING 1encodes a polygalacturonase that modifies cell wall structure and drought tolerance in rice. New Phytol, 229(2): 890-901.
[93]	Zhang J J, Wu S Y, Jiang L, Wang J L, Zhang X, Guo X P, Wu C Y, Wan J M. 2015. A detailed analysis of the leaf rolling mutant sll2 reveals complex nature in regulation of bulliform cell development in rice (Oryza sativa L.). Plant Biol, 17(2): 437-448.
[94]	Zhang J S, Zhang H, Srivastava A K, Pan Y J, Bai J J, Fang J J, Shi H Z, Zhu J K. 2018. Knockdown of rice microRNA166 confers drought resistance by causing leaf rolling and altering stem xylem development. Plant Physiol, 176(3): 2082-2094. PMID
[95]	Zhang T P, Li C Y, Li D X, Liu Y, Yang X H. 2020. Roles of YABBY transcription factors in the modulation of morphogenesis, development, and phytohormone and stress responses in plants. J Plant Res, 133(6): 751-763. PMID
[96]	Zhao S Q, Xiang J J, Xue H W. 2013. Studies on the rice LEAF INCLINATION1 (LC1), an IAA-amido synthetase, reveal the effects of auxin in leaf inclination control. Mol Plant, 6(1): 174-187.
[97]	Zhao S S, Zhao L, Liu F X, Wu Y Z, Zhu Z F, Sun C Q, Tan L B. 2016. NARROW AND ROLLED LEAF 2 regulates leaf shape, male fertility, and seed size in rice. J Integr Plant Biol, 58(12): 983-996.
[98]	Zhou L G, Liu Z C, Liu Y H, Kong D Y, Li T F, Yu S W, Mei H W, Xu X Y, Liu H Y, Chen L, Luo L J. 2016. A novel gene OsAHL1 improves both drought avoidance and drought tolerance in rice. Sci Rep, 6(1): 30264.
[99]	Zhou Z M, Fan J B, Zhang J, Yang Y M, Zhang Y F, Zan X F, Li X H, Wan J L, Gao X L, Chen R J, Huang Z J, Xu Z J, Li L H. 2022. OsMLP423 is a positive regulator of tolerance to drought and salt stresses in rice. Plants, 11(13): 1653.
[100]	Zoghi Z, Hosseini S M, Kouchaksaraei M T, Kooch Y, Guidi L. 2019. The effect of biochar amendment on the growth, morphology and physiology of Quercus castaneifolia seedlings under water- deficit stress. Eur J Forest Res, 138(6): 967-979.
[101]	Zou L P, Sun X H, Zhang Z G, Liu P, Wu J X, Tian C J, Qiu J L, Lu T G. 2011. Leaf rolling controlled by the homeodomain leucine zipper class IV gene Roc5 in rice. Plant Physiol, 156(3): 1589-1602.
[102]	Zou L P, Zhang Z G, Qi D F, Peng M, Lu T G. 2014. Cytological mechanisms of leaf rolling in rice. Crop Sci, 54(1): 198-209.
[103]	Zu X F, Lu Y K, Wang Q Q, Chu P F, Miao W, Wang H Q, La H G. 2017. A new method for evaluating the drought tolerance of upland rice cultivars. Crop J, 5(6): 488-498.

Crop	Water required
Crop	Depth (cm)	Quantity (L/kg)	Depth (cm)	Depth (cm)	Quantity (L/plant)
Rice	95‒100	2 497	182	90‒250	23.95
Wheat	‒	1 350	75	45‒65	6.91
Maize	40‒45	1 222	84	50‒80	‒
Potato	‒	287	88	50‒70	30.11
Cotton	60‒75	10 000	‒	70‒130	‒
Groundnut	60‒65	‒	‒	50‒70	17.84

Crop	Water required
Crop	Depth (cm)	Quantity (L/kg)	Depth (cm)	Depth (cm)	Quantity (L/plant)
Rice	95‒100	2 497	182	90‒250	23.95
Wheat	‒	1 350	75	45‒65	6.91
Maize	40‒45	1 222	84	50‒80	‒
Potato	‒	287	88	50‒70	30.11
Cotton	60‒75	10 000	‒	70‒130	‒
Groundnut	60‒65	‒	‒	50‒70	17.84

Gene abbreviation	Gene full name	Transcription factor/ Gene regulator	Functional role in leaf rolling	Reference
ADL1	ADAXIALIZED LEAF1	Calpain-like cysteine protease	Involved in abaxial leaf rolling	Hibara et al, 2009
SLL1	SHALLOT-LIKE1	MYB family transcriptional factor class SHAQKYF	Controls the growth of sclerenchyma cells	Zhang et al, 2009
ACL1	abaxially curled leaf 1	Unidentified protein	Determines the development of leaves	Li et al, 2010
NRL1	NARROW AND ROLLED LEAF 1	Cellulose synthase like protein D4	Regulates cell formation	Hu et al, 2010
CFL1	CURLY FLAG LEAF1	A homeodomain transcription factor class IV	Governs cuticle development	Wu et al, 2011; Li et al, 2022
ROC5	Rice outermost cell-specific gene5	A homeodomain leucine zipper class IV transcriptional factor	Regulates the formation of bulliform cells	Zou et al, 2011
RL14	Rolling-leaf14	2OG-Fe (II) oxygenase	Controls the secondary cell wall formation	Fang et al, 2012
LC1	LEAF INCLINATION1	T-DNA insert in LOC_Os07g38664	Directs cell division	Zhao et al, 2013
OsZHD1	zinc finger homeodomain 1	ZF-HD transcription factor	Participates in abaxial rolling	Xu et al, 2014
SLL2	SHALLOT-LIKE2	Unidentified plant-specific protein	Controls the size and shape of bulliform cell	Zhang et al, 2015
REL1	Rolled and Erect Leaf 1	Unknown protein	Positive regulator of leaf rolling	Chen et al, 2015
OsI-BAK1	Brassinosteroid Insensitive 1-Associated Kinase 1	Unknown	Involved in BR signaling pathway	Khew et al, 2015
OsARF18	AUXIN RESPONSE FACTOR18	Target of mirna160	Involved in auxin signaling	Huang et al, 2016
REL2	Rolled and Erect Leaf 2	An unknown protein containing DUF630 and DUF632 domains	Defines the leaf shape	Yang et al, 2016
OsLBD3-7	lateral organ boundary domain 3-7	DUF260 domain protein	Serves as an activator of transcription	Pina et al, 2016
CLD1/SRL1	CURLED LEAF AND DWARF 1	GPI anchored protein	Controls osmotic adjustment and cell wall integrity	Li et al, 2017
OsRRK1	Rop-interesting receptor-like cytoplasmic kinase 1	Unidentified	Causes adaxial rolling by controlling the size of bulliform cells	Ma et al, 2017
RFS	Rolled Fine Striped	CHD3/Mi-2	Regulates leaf polarity	Cho et al, 2018
OSHB4	HOMEODOMAIN CONTAINING PROTEIN 4	HD-ZIP class III gene	Responsible for adaxial curling due to a decrease in number of bulliform cells	Zhang et al, 2018
OsCHR4	Chromatin remodeling factor 4	CHD3 chromatin modeler	Encourages thin and curled leaf phenotype with thicker cuticular wax	Guo et al, 2019
PSL1	PHOTO-SENSITIVE LEAF ROLLING 1	Cell wall-localized polygalacturonase	Enhances drought tolerance by modifying the cell wall and leaf rolling phenotype	Zhang et al, 2021
SRL3	SEMI-ROLLED LEAF 3	Novel gene with unknown protein	Responsible for abnormal development of bulliform and sclerenchyma cells	Yu X Q et al, 2022
ditl1	Drought insensitive TILLING line 1	Deletion of one nucleotide on LOC_Os05g48260 gene	Decreases water loss and leaf rolling by accumulating cuticular wax at epidermal cells	Choi et al, 2022
OsMLP423	Major latex protein 423	Belongs to major latex protein family	Heightens drought tolerance by curling leaves	Zhou et al, 2022

Gene abbreviation	Gene full name	Transcription factor/ Gene regulator	Functional role in leaf rolling	Reference
ADL1	ADAXIALIZED LEAF1	Calpain-like cysteine protease	Involved in abaxial leaf rolling	Hibara et al, 2009
SLL1	SHALLOT-LIKE1	MYB family transcriptional factor class SHAQKYF	Controls the growth of sclerenchyma cells	Zhang et al, 2009
ACL1	abaxially curled leaf 1	Unidentified protein	Determines the development of leaves	Li et al, 2010
NRL1	NARROW AND ROLLED LEAF 1	Cellulose synthase like protein D4	Regulates cell formation	Hu et al, 2010
CFL1	CURLY FLAG LEAF1	A homeodomain transcription factor class IV	Governs cuticle development	Wu et al, 2011; Li et al, 2022
ROC5	Rice outermost cell-specific gene5	A homeodomain leucine zipper class IV transcriptional factor	Regulates the formation of bulliform cells	Zou et al, 2011
RL14	Rolling-leaf14	2OG-Fe (II) oxygenase	Controls the secondary cell wall formation	Fang et al, 2012
LC1	LEAF INCLINATION1	T-DNA insert in LOC_Os07g38664	Directs cell division	Zhao et al, 2013
OsZHD1	zinc finger homeodomain 1	ZF-HD transcription factor	Participates in abaxial rolling	Xu et al, 2014
SLL2	SHALLOT-LIKE2	Unidentified plant-specific protein	Controls the size and shape of bulliform cell	Zhang et al, 2015
REL1	Rolled and Erect Leaf 1	Unknown protein	Positive regulator of leaf rolling	Chen et al, 2015
OsI-BAK1	Brassinosteroid Insensitive 1-Associated Kinase 1	Unknown	Involved in BR signaling pathway	Khew et al, 2015
OsARF18	AUXIN RESPONSE FACTOR18	Target of mirna160	Involved in auxin signaling	Huang et al, 2016
REL2	Rolled and Erect Leaf 2	An unknown protein containing DUF630 and DUF632 domains	Defines the leaf shape	Yang et al, 2016
OsLBD3-7	lateral organ boundary domain 3-7	DUF260 domain protein	Serves as an activator of transcription	Pina et al, 2016
CLD1/SRL1	CURLED LEAF AND DWARF 1	GPI anchored protein	Controls osmotic adjustment and cell wall integrity	Li et al, 2017
OsRRK1	Rop-interesting receptor-like cytoplasmic kinase 1	Unidentified	Causes adaxial rolling by controlling the size of bulliform cells	Ma et al, 2017
RFS	Rolled Fine Striped	CHD3/Mi-2	Regulates leaf polarity	Cho et al, 2018
OSHB4	HOMEODOMAIN CONTAINING PROTEIN 4	HD-ZIP class III gene	Responsible for adaxial curling due to a decrease in number of bulliform cells	Zhang et al, 2018
OsCHR4	Chromatin remodeling factor 4	CHD3 chromatin modeler	Encourages thin and curled leaf phenotype with thicker cuticular wax	Guo et al, 2019
PSL1	PHOTO-SENSITIVE LEAF ROLLING 1	Cell wall-localized polygalacturonase	Enhances drought tolerance by modifying the cell wall and leaf rolling phenotype	Zhang et al, 2021
SRL3	SEMI-ROLLED LEAF 3	Novel gene with unknown protein	Responsible for abnormal development of bulliform and sclerenchyma cells	Yu X Q et al, 2022
ditl1	Drought insensitive TILLING line 1	Deletion of one nucleotide on LOC_Os05g48260 gene	Decreases water loss and leaf rolling by accumulating cuticular wax at epidermal cells	Choi et al, 2022
OsMLP423	Major latex protein 423	Belongs to major latex protein family	Heightens drought tolerance by curling leaves	Zhou et al, 2022