Recent Insights into Signaling Responses to Cope Drought Stress in Rice
Received date: 2021-04-14
Accepted date: 2021-08-02
Online published: 2022-02-09
Drought is one of the hot topics needing urgent attention in the current era of climate change. It massively disturbs the rice growth and productivity and is becoming a serious threat. The drought avoidance strategies in rice include stomatal closure, cellular adaptation and changes in root development. Moreover, the endogenous plant hormones (abscisic acid and jasmonic acid) and reactive oxygen species have paramount importance in drought tolerance in rice. The drought tolerance induces modification in biochemical, molecular and physiological properties of plants. At the molecular level, expression of several transcription-factors is modulated which further determine the activation of drought responsive gene families. Mitogen activated protein kinases and Ca signaling pathways initiate an array of signaling cascade for mediating the gene expression in rice. Approaches, conventional breeding methods combined with modern emerging techniques such as genetic engineering, to improve rice drought tolerance were discussed. This review provided recent insights into major regulatory factors against drought stress, signaling mechanisms and molecular engineering strategies (including conventional transgenic and recent genome editing approaches) to induce drought tolerance in rice.
Key words： drought stress; rice; signaling response; regulatory factor
Muhammad Mahran Aslam, Muhammad Abdul Rehman Rashid, Mohammad Aquil Siddiqui, Muhammad Tahir Khan, Fozia Farhat, Shafquat Yasmeen, Imtiaz Ahmad Khan, Shameem Raja, Fatima Rasool, Mahboob Ali Sial, Zhao Yan . Recent Insights into Signaling Responses to Cope Drought Stress in Rice[J]. Rice Science, 2022 , 29(2) : 105 -117 . DOI: 10.1016/j.rsci.2021.08.001
| [1] | Ahmad P, Rasool S, Gul A, Sheikh S A, Akram N A, Ashraf M, Kazi A M, Gucel S. 2016. Jasmonates: Multifunctional roles in stress tolerance. Front Plant Sci, 7: 813. |
| [2] | Ahmed S, Rashid M A R, Zafar S A, Azhar M T, Waqas M, Uzair M, Rana I A, Azeem F, Chung G, Ali Z, Atif R M. 2021. Genome- wide investigation and expression analysis of APETALA-2 transcription factor subfamily reveals its evolution, expansion and regulatory role in abiotic stress responses in indica rice (Oryza sativa L. ssp. indica). Genomics, 113(1): 1029-1043. |
| [3] | An J, Li Q X, Yang J J, Zhang G Q, Zhao Z X, Wu Y Z, Wang Y, Wang W. 2019. Wheat F-box protein TaFBA1 positively regulates plant drought tolerance but negatively regulates stomatal closure. Front Plant Sci, 10: 1242. |
| [4] | Bai F W, Matton D P. 2018. The Arabidopsis Mitogen-Activated Protein Kinase Kinase Kinase 20 (MKKK20) C-terminal domain interacts with MKK3 and harbors a typical DEF mammalian MAP kinase docking site. Plant Signal Behav, 13(8): e1503498. |
| [5] | Baltes N J, Gil-Humanes J, Cermak T, Atkins P A, Voytas D F. 2014. DNA replicons for plant genome engineering. Plant Cell, 26(1): 151-163. |
| [6] | Basu S, Ramegowda V, Kumar A, Pereira A. 2016. Plant adaptation to drought stress. F1000Research, 5: 1554. |
| [7] | Bertolino L T, Caine R S, Gray J E. 2019. Impact of stomatal density and morphology on water-use efficiency in a changing world. Front Plant Sci, 10: 225. |
| [8] | Biswal A K, Mangrauthia S K, Reddy M R, Yugandhar P. 2019. CRISPR mediated genome engineering to develop climate smart rice: Challenges and opportunities. Semin Cell Dev Biol, 96: 100-106. |
| [9] | Borah L, Baruah K K. 2016. Effects of foliar application of plant growth hormone on methane emission from tropical rice paddy. Agric Ecosyst Environ, 233: 75-84. |
| [10] | Bray E A, Bailey-Serres J, Weretilnyk E. 2000. Responses to abiotic stresses. In: Gruissem W, Buchannan B, Jones R. Biochemistry and Molecular Biology of Plants. Rockville, MD, USA: American Society of Plant Physiologists: 1158-1249. |
| [11] | Caine R S, Yin X J, Sloan J, Harrison E L, Mohammed U, Fulton T, Biswal A K, Dionora J, Chater C C, Coe R A, Bandyopadhyay A, Murchie E H, Swarup R, Quick W P, Gray J E. 2019. Rice with reduced stomatal density conserves water and has improved drought tolerance under future climate conditions. New Phytol, 221(1): 371-384. |
| [12] | Chini A, Fonseca S, Fernández G, Adie B, Chico J M, Lorenzo O, García-Casado G, López-Vidriero I, Lozano F M, Ponce M R, Micol J L, Solano R. 2007. The JAZ family of repressors is the missing link in jasmonate signalling. Nature, 448: 666-671. |
| [13] | Comas L H, Becker S R, Cruz V M V, Byrne P F, Dierig D A. 2013. Root traits contributing to plant productivity under drought. Front Plant Sci, 4: 442. |
| [14] | Crawford A J, McLachlan D H, Hetherington A M, Franklin K A. 2012. High temperature exposure increases plant cooling capacity. Curr Biol, 22(10): R396-R397. |
| [15] | Danquah A, de Zelicourt A, Colcombet J, Hirt H. 2014. The role of ABA and MAPK signaling pathways in plant abiotic stress responses. Biotechnol Adv, 32(1): 40-52. |
| [16] | Das K, Roychoudhury A. 2014. Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci, 2: 53. |
| [17] | de Carvalho M H C. 2008. Drought stress and reactive oxygen species: Production, scavenging and signaling. Plant Signal Behav, 3(3): 156-165. |
| [18] | Dhakarey R, Raorane M L, Treumann A, Peethambaran P K, Schendel R R, Sahi V P, Hause B, Bunzel M, Henry A, Kohli A, Riemann M. 2017. Physiological and proteomic analysis of the rice mutant cpm2 suggests a negative regulatory role of jasmonic acid in drought tolerance. Front Plant Sci, 8: 1903. |
| [19] | Din J U, Khan S U, Khan A, Naveed S. 2015. Effect of exogenously applied kinetin and glycinebetaine on metabolic and yield attributes of rice (Oryza sativa L.) under drought stress. Emir J Food Agric, 27(1): 75-81. |
| [20] | Ding W N, Wu J, Ye J, Zheng W J, Wang S S, Zhu X N, Zhou J Q, Pan Z C, Zhang B T, Zhu S H. 2018. A Pelota-like gene regulates root development and defence responses in rice. Ann Bot, 122(3): 359-371. |
| [21] | Dixit S, Huang B E, Sta Cruz M T, Maturan P T, Ontoy J C E, Kumar A. 2014. QTLs for tolerance of drought and breeding for tolerance of abiotic and biotic stress: An integrated approach. PLoS One, 9(10): e109574. |
| [22] | Dong T, Park Y, Hwang I. 2015. Abscisic acid: Biosynthesis, inactivation, homoeostasis and signalling. Essays Biochem, 58: 29-48. |
| [23] | Du H, Chang Y, Huang F, Xiong L Z. 2015. GID1 modulates stomatal response and submergence tolerance involving abscisic acid and gibberellic acid signaling in rice. J Integr Plant Biol, 57(11): 954-968. |
| [24] | Elliott J, Deryng D, Müller C, Frieler K, Konzmann M, Gerten D, Glotter M, Flörke M, Wada Y, Best N, Eisner S, Fekete B M, Folberth C, Foster I, Gosling S N, Haddeland I, Khabarov N, Ludwig F, Masaki Y, Olin S, Rosenzweig C, Ruane A C, Satoh Y, Schmid E, Stacke T, Tang Q H, Wisser D. 2014. Constraints and potentials of future irrigation water availability on agricultural production under climate change. Proc Natl Acad Sci USA, 111(9): 3239-3244. |
| [25] | Fahad S, Bajwa A A, Nazir U, Anjum S A, Farooq A, Zohaib A, Sadia S, Nasim W, Adkins S, Saud S, Ihsan M Z, Alharby H, Wu C, Wang D P, Huang J L. 2017. Crop production under drought and heat stress: Plant responses and management options. Front Plant Sci, 8: 1147. |
| [26] | Farooq M, Hussain M, Wahid A, Siddique K H M. 2012. Drought stress in plants:An overview. In: Aroca R. Plant Responses to Drought Stress. Berlin, Germany: Springer: 1-33. |
| [27] | Franz S, Ehlert B, Liese A, Kurth J, Cazalé A C, Romeis T. 2011. Calcium-dependent protein kinase CPK 21 functions in abiotic stress response in Arabidopsis thaliana. Mol Plant, 4(1): 83-96. |
| [28] | Fukao T, Bailey-Serres J. 2008. Submergence tolerance conferred by Sub1A is mediated by SLR1 and SLRL1 restriction of gibberellin responses in rice. Proc Natl Acad Sci USA, 105: 16814-16819. |
| [29] | Gao F M, Wen W E, Liu J D, Rasheed A, Yin G H, Xia X C, Wu X X, He Z H. 2015. Genome-wide linkage mapping of QTL for yield components, plant height and yield-related physiological traits in the Chinese wheat cross Zhou 8425B/Chinese Spring. Front Plant Sci, 6: 1099. |
| [30] | Gu Q H, Lin R L. 2010. Heavy metals zinc, cadmium, and copper stimulate pulmonary sensory neurons via direct activation of TRPA1. J Appl Physiol, 108(4): 891-897. |
| [31] | Gupta A, Rico-Medina A, Caño-Delgado A I. 2020. The physiology of plant responses to drought. Science, 368: 266-269. |
| [32] | Gupta B, Huang B. 2014. Mechanism of salinity tolerance in plants: Physiological, biochemical, and molecular characterization. Int J Genomics, 2014: 701596. |
| [33] | Gustin M C, Albertyn J, Alexander M, Davenport K. 1998. MAP kinase pathways in the yeast Saccharomyces cerevisiae. Microbiol Mol Biol Rev, 62(4): 1264-1300. |
| [34] | Haak D C, Fukao T, Grene R, Hua Z H, Ivanov R, Perrella G, Li S. 2017. Multilevel regulation of abiotic stress responses in plants. Front Plant Sci, 8: 1564. |
| [35] | Hadiarto T, Tran L S P. 2011. Progress studies of drought-responsive genes in rice. Plant Cell Rep, 30(3): 297-310. |
| [36] | Hasanuzzaman M, Alam M M, Rahman A, Hasanuzzaman M, Nahar K, Fujita M. 2014. Exogenous proline and glycine betaine mediated upregulation of antioxidant defense and glyoxalase systems provides better protection against salt-induced oxidative stress in two rice (Oryza sativa L.) varieties. Biomed Res Int, 2014: 757219. |
| [37] | Hasanuzzaman M, Anee T I, Bhuiyan T F, Nahar K, Fujita M. 2019. Emerging role of osmolytes in enhancing abiotic stress tolerance in rice. In: Hasanuzzaman M, Fujita M, Nahar K, Biswas J K. Advances in Rice Research for Abiotic Stress Tolerance. London, UK: Woodhead Publishing: 677-708. |
| [38] | Heber U. 2002. Irrungen, Wirrungen? The Mehler reaction in relation to cyclic electron transport in C3 plants. Photosynth Res, 73: 223-231. |
| [39] | Henry A, Cal A J, Batoto T C, Torres R O, Serraj R. 2012. Root attributes affecting water uptake of rice (Oryza sativa) under drought. J Exp Bot, 63(13): 4751-4763. |
| [40] | Hou X, Xie K B, Yao J L, Qi Z Y, Xiong L Z. 2009. A homolog of human ski-interacting protein in rice positively regulates cell viability and stress tolerance. Proc Natl Acad Sci USA, 106(15): 6410-6415. |
| [41] | Hu Y, Wu Q Y, Peng Z, Sprague S A, Wang W, Park J, Akhunov E, Jagadish K S V, Nakata P A, Cheng N H, Hirschi K D, White F F, Park S. 2017. Silencing of OsGRXS17 in rice improves drought stress tolerance by modulating ROS accumulation and stomatal closure. Sci Rep, 7(1): 15950. |
| [42] | Huang L Y, Wang Y X, Wang W S, Zhao X Q, Qin Q, Sun F, Hu F Y, Zhao Y, Li Z C, Fu B Y, Li Z K. 2018. Characterization of transcription factor gene OsDRAP1 conferring drought tolerance in rice. Front Plant Sci, 9: 94. |
| [43] | Jiang J J, Ma S H, Ye N H, Jiang M, Cao J S, Zhang J H. 2017. WRKY transcription factors in plant responses to stresses. J Integr Plant Biol, 59(2): 86-101. |
| [44] | Jung H, Chung P J, Park S H, Redillas M C F R, Kim Y S, Suh J W, Kim J K. 2017. Overexpression of OsERF48 causes regulation of OsCML16, a calmodulin-like protein gene that enhances root growth and drought tolerance. Plant Biotechnol J, 15(10): 1295-1308. |
| [45] | Kartika K, Jun-Ichi S, Benyamin L, Shin Y, Andi W, Sabaruddin K, Laily I W, Erna S, Yoshihiro N. 2020. Morpho-physiological response of Oryza glaberrima to gradual soil drying. Rice Sci, 27(1): 67-74. |
| [46] | Kim H, Lee K, Hwang H, Bhatnagar N, Kim D Y, Yoon I S, Byun M O, Kim S T, Jung K H, Kim B G. 2014. Overexpression of PYL5 in rice enhances drought tolerance, inhibits growth, and modulates gene expression. J Exp Bot, 65(2): 453-464. |
| [47] | Khan A, Pan X D, Najeeb U, Tan D K Y, Fahad S, Zahoor R, Luo H H. 2018. Coping with drought: stress and adaptive mechanisms, and management through cultural and molecular alternatives in cotton as vital constituents for plant stress resilience and fitness. Biol Res, 51(1): 47. |
| [48] | Ku Y S, Sintaha M, Cheung M Y, Lam H M. 2018. Plant hormone signaling crosstalks between biotic and abiotic stress responses. Int J Mol Sci, 19(10): 3206. |
| [49] | Kuromori T, Miyaji T, Yabuuchi H, Shimizu H, Sugimoto E, Kamiya A, Moriyama Y, Shinozaki K. 2010. ABC transporter AtABCG25 is involved in abscisic acid transport and responses. Proc Natl Acad Sci USA, 107(5): 2361-2366. |
| [50] | Kusumi K, Hirotsuka S, Kumamaru T, Iba K. 2012. Increased leaf photosynthesis caused by elevated stomatal conductance in a rice mutant deficient in SLAC1, a guard cell anion channel protein. J Exp Bot, 63(15): 5635-5644. |
| [51] | Lazar A, Coll A, Dobnik D, Baebler S, Bedina-Zavec A, Zel J, Gruden K. 2014. Involvement of potato (Solanum tuberosum L.) MKK6 in response to Potato virus Y. PLoS One, 9(8): e104553. |
| [52] | Lee D K, Jung H, Jang G, Jeong J S, Kim Y S, Ha S H, Do Choi Y, Kim J K. 2016. Overexpression of the OsERF71 transcription factor alters rice root structure and drought resistance. Plant Physiol, 172(1): 575-588. |
| [53] | Li J J, Guo X, Zhang M H, Wang X, Zhao Y, Yin Z G, Zhang Z Y, Wang Y M, Xiong H Y, Zhang H L, Todorovska E, Li Z C. 2018. OsERF71 confers drought tolerance via modulating ABA signaling and proline biosynthesis. Plant Sci, 270: 131-139. |
| [54] | Li Y, Zhou Y, Guo S W, Shen Q R. 2007. Effects of different N forms on root morphology and water absorption of lowland and upland rice plants. Chin J Rice Sci, 21(3): 294-298. (in Chinese with English abstract) |
| [55] | Liu Y K, He C Z. 2017. A review of redox signaling and the control of MAP kinase pathway in plants. Redox Biol, 11: 192-204. |
| [56] | Lou D J, Wang H P, Liang G, Yu D Q. 2017. OsSAPK2 confers abscisic acid sensitivity and tolerance to drought stress in rice. Front Plant Sci, 8: 993. |
| [57] | Ma S Q, Tang N, Li X, Xie Y J, Xiang D H, Fu J, Shen J Q, Yang J, Tu H F, Li X H, Hu H H, Xiong L Z. 2019. Reversible histone H2B monoubiquitination fine-tunes abscisic acid signaling and drought response in rice. Mol Plant, 12(2): 263-277. |
| [58] | Mahrookashani A, Siebert S, Hüging H, Ewert F. 2017. Independent and combined effects of high temperature and drought stress around anthesis on wheat. J Agron Crop Sci, 203(6): 453-463. |
| [59] | Mehrotra R, Bhalothia P, Bansal P, Basantani M K, Bharti V, Mehrotra S. 2014. Abscisic acid and abiotic stress tolerance: Different tiers of regulation. J Plant Physiol, 171(7): 486-496. |
| [60] | Mishra R, Joshi R K, Zhao K J. 2018. Genome editing in rice: Recent advances, challenges, and future implications. Front Plant Sci, 9: 1361. |
| [61] | Mittal S, Mallikarjuna M G, Rao A R, Jain P A, Dash P K, Thirunavukkarasu N. 2017. Comparative analysis of CDPK family in maize, Arabidopsis, rice, and sorghum revealed potential targets for drought tolerance improvement. Front Chem, 5: 115. |
| [62] | Mittler R. 2002. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci, 7(9): 405-410. |
| [63] | Mori I C, Murata Y, Yang Y Z, Munemasa S, Wang Y F, Andreoli S, Tiriac H, Alonso J M, Harper J F, Ecker J R, Kwak J M, Schroeder J I. 2006. CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca2+-permeable channels and stomatal closure. PLoS Biol, 4(10): e327. |
| [64] | Muthayya S, Sugimoto J D, Montgomery S, Maberly G F. 2014. An overview of global rice production, supply, trade, and consumption. Ann N Y Acad Sci, 1324(1): 7-14. |
| [65] | Noctor G, Veljovic-Jovanovic S, Driscoll S, Novitskaya L, Foyer C H. 2002. Drought and oxidative load in the leaves of C3 plants: A predominant role for photorespiration? Ann Bot, 89(7): 841-850. |
| [66] | Ogata T, Ishizaki T, Fujita M, Fujita Y. 2020. CRISPR/Cas9- targeted mutagenesis of OsERA1 confers enhanced responses to abscisic acid and drought stress and increased primary root growth under nonstressed conditions in rice. PLoS One, 15(12): e0243376. |
| [67] | Papanatsiou M, Petersen J, Henderson L, Wang Y, Christie J M, Blatt M R. 2019. Optogenetic manipulation of stomatal kinetics improves carbon assimilation, water use, and growth. Science, 363: 1456-1459. |
| [68] | Quan R D, Wang J, Hui J, Bai H B, Lü X L, Zhu Y X, Zhang H W, Zhang Z J, Li S H, Huang R F. 2018. Improvement of salt tolerance using wild rice genes. Front Plant Sci, 8: 2269. |
| [69] | Ramegowda V, Basu S, Krishnan A, Pereira A. 2014. Rice GROWTH UNDER DROUGHT KINASE is required for drought tolerance and grain yield under normal and drought stress conditions. Plant Physiol, 166(3): 1634-1645. |
| [70] | Rebouillat J, Dievart A, Verdeil J L, Escoute J, Giese G, Breitler J C, Gantet P, Espeout S, Guiderdoni E, Périn C. 2009. Molecular genetics of rice root development. Rice, 2(1): 15-34. |
| [71] | Sahebi M, Hanafi M M, Rafii M Y, Mahmud T M M, Azizi P, Osman M, Abiri R, Taheri S, Kalhori N, Shabanimofrad M, Miah G, Atabaki N. 2018. Improvement of drought tolerance in rice (Oryza sativa L.): Genetics, genomic tools, and the WRKY gene family. Biomed Res Int, 2018: 3158474. |
| [72] | Santosh Kumar V V, Verma R K, Yadav S K, Yadav P, Watts A, Rao M V, Chinnusamy V. 2020. CRISPR-Cas9 mediated genome editing of drought and salt tolerance (OsDST) gene in indica mega rice cultivar MTU1010. Physiol Mol Biol Plants, 26(6): 1099-1110. |
| [73] | Saud S, Fahad S, Chen Y J, Ihsan M Z, Hammad H M, Nasim W, Amanullah Jr, Arif M, Alharby H. 2017. Effects of nitrogen supply on water stress and recovery mechanisms in Kentucky bluegrass plants. Front Plant Sci, 8: 983. |
| [74] | Schulz P, Herde M, Romeis T. 2013. Calcium-dependent protein kinases: Hubs in plant stress signaling and development. Plant Physiol, 163(2): 523-530. |
| [75] | Serraj R, McNally K L, Slamet-Loedin I, Kohli A, Haefele S M, Atlin G, Kumar A. 2011. Drought resistance improvement in rice: An integrated genetic and resource management strategy. Plant Prod Sci, 14(1): 1-14. |
| [76] | Shi S J, Li S G, Asim M, Mao J J, Xu D Z, Ullah Z, Liu G S, Wang Q, Liu H B. 2018. The Arabidopsis calcium-dependent protein kinases (CDPKs) and their roles in plant growth regulation and abiotic stress responses. Int J Mol Sci, 19(7): 1900. |
| [77] | Silva D V, Cabral C M, Ferreira E A, de Carvalho F P, dos Santos J B, Dombroski J L D. 2018. Anatomical adaptations to different soil moisture contents in palisade grass and smooth pigweed. Rev Ceres Vicosa, 65(4): 306-313. |
| [78] | Tabassum J, Ahmad S, Hussain B, Mawia A M, Zeb A, Luo J. 2021. Applications and potential of genome-editing systems in rice improvement: Current and future perspectives. Agronomy, 11(7): 1359. |
| [79] | Todaka D, Shinozaki K, Yamaguchi-Shinozaki K. 2015. Recent advances in the dissection of drought-stress regulatory networks and strategies for development of drought-tolerant transgenic rice plants. Front Plant Sci, 6: 84. |
| [80] | Ullah A, Sun H, Yang X Y, Zhang X L. 2017. Drought coping strategies in cotton: Increased crop per drop. Plant Biotechnol J, 15(3): 271-284. |
| [81] | Usman B, Nawaz G, Zhao N, Liao S Y, Liu Y G, Li R B. 2020. Precise editing of the OsPYL9 gene by RNA-guided Cas9 nuclease confers enhanced drought tolerance and grain yield in rice (Oryza sativa L.) by regulating circadian rhythm and abiotic stress responsive proteins. Int J Mol Sci, 21(21): 7854. |
| [82] | Verma V, Ravindran P, Kumar P P. 2016. Plant hormone-mediated regulation of stress responses. BMC Plant Biol, 16: 86. |
| [83] | Wang B, Zhong Z H, Wang X, Han X Y, Yu D S, Wang C G, Song W Q, Zheng X L, Chen C B, Zhang Y. 2020. Knockout of the OsNAC006 transcription factor causes drought and heat sensitivity in rice. Int J Mol Sci, 21(7): 2288. |
| [84] | Wang H Z, Zhang L H, Ma J, Li X Y, Li Y, Zhang R P, Wang R Q. 2010. Effects of water stress on reactive oxygen species generation and protection system in rice during grain-filling stage. Agric Sci China, 9(5): 633-641. |
| [85] | Wang Y, Lu Y Y, Guo Z Y, Ding Y F, Ding C Q. 2020. RICE CENTRORADIALIS 1, a TFL1-like gene, responses to drought stress and regulates rice flowering transition. Rice, 13(1): 70. |
| [86] | Wang Z, Wang F X, Hong Y C, Yao J J, Ren Z Z, Shi H Z, Zhu J K. 2018. The flowering repressor SVP confers drought resistance in Arabidopsis by regulating abscisic acid catabolism. Mol Plant, 11(9): 1184-1197. |
| [87] | Wei S Y, Hu W, Deng X M, Zhang Y Y, Liu X D, Zhao X D, Luo Q C, Jin Z Y, Li Y, Zhou S Y, Sun T, Wang L Z, Yang G X, He G Y. 2014. A rice calcium-dependent protein kinase OsCPK9 positively regulates drought stress tolerance and spikelet fertility. BMC Plant Biol, 14: 133. |
| [88] | Wu D, Guo Z L, Ye J L, Feng H, Liu J X, Chen G X, Zheng J S, Yan D M, Yang X Q, Xiong X, Liu Q, Niu Z Y, Gray A P, Doonan J H, Xiong L Z, Yang W N. 2019. Combining high-throughput micro-CT-RGB phenotyping and genome-wide association study to dissect the genetic architecture of tiller growth in rice. J Exp Bot, 70(2): 545-561. |
| [89] | Xiong H Y, Yu J P, Miao J L, Li J J, Zhang H L, Wang X, Liu P L, Zhao Y, Jiang C H, Yin Z G, Li Y, Guo Y, Fu B Y, Wang W S, Li Z K, Ali J, Li Z C. 2018. Natural variation in OsLG3 increases drought tolerance in rice by inducing ROS scavenging. Plant Physiol, 178(1): 451-467. |
| [90] | Xu Z Z, Jiang Y L, Jia B R, Zhou G S. 2016. Elevated-CO2 response of stomata and its dependence on environmental factors. Front Plant Sci, 7: 657. |
| [91] | Yamaguchi-Shinozaki K, Shinozaki K. 2006. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol, 57: 781-803. |
| [92] | Yang S Y, Hao D L, Jin M, Li Y, Liu Z T, Huang Y N, Chen T X, Su Y H. 2020. Internal ammonium excess induces ROS-mediated reactions and causes carbon scarcity in rice. BMC Plant Biol, 20(1): 143. |
| [93] | You J, Chan Z L. 2015. ROS regulation during abiotic stress responses in crop plants. Front Plant Sci, 6: 1092. |
| [94] | Zafar S A, Zaidi S S E, Gaba Y, Singla-Pareek S L, Dhankher O P, Li X Y, Mansoor S, Pareek A. 2020. Engineering abiotic stress tolerance via CRISPR/Cas-mediated genome editing. J Exp Bot, 71(2): 470-479. |
| [95] | Zaman Q U, Li C, Cheng H T, Hu Q. 2019. Genome editing opens a new era of genetic improvement in polyploid crops. Crop J, 7(2): 141-150. |
| [96] | Zhang A, Ren H M, Tan Y Q, Qi G N, Yao F Y, Wu G L, Yang L W, Hussain J, Sun S J, Wang Y F. 2016. S-type anion channels SLAC1 and SLAH 3 function as essential negative regulators of inward K+ channels and stomatal opening in Arabidopsis. Plant Cell, 28(4): 949-955. |
| [97] | Zhang H, Li Y Y, Zhu J K. 2018. Developing naturally stress- resistant crops for a sustainable agriculture. Nat Plants, 4(12): 989-996. |
| [98] | Zhang J H, Schurr U, Davies W J. 1987. Control of stomatal behaviour by abscisic acid which apparently originates in the roots. J Exp Bot, 38(7): 1174-1181. |
| [99] | Zhou H, He M, Li J, Chen L, Huang Z F, Zheng S Y, Zhu L Y, Ni E D, Jiang D G, Zhao B R, Zhuang C X. 2016. Development of commercial thermo-sensitive genic male sterile rice accelerates hybrid rice breeding using the CRISPR/Cas9-mediated TMS5 editing system. Sci Rep, 6: 37395. |
| [100] | Zhou H Y, Ren S Y, Han Y F, Zhang Q, Qin L, Xing Y. 2017. Identification and analysis of mitogen-activated protein kinase (MAPK) cascades in Fragaria vesca. Int J Mol Sci, 18(8): 1766. |
/
| 〈 |
|
〉 |