Progress on Improving Rice Yield under Abiotic Stress by Genetic Engineering

doi:10.3969/j.issn.1006-8082.2023.03.003

Abstract

Abstract:

Abiotic stresses such as drought, salt, low temperature and high temperature seriously affect the growth, development and yield of rice. Increasing rice yield under abiotic stress is of great practical significance for ensuring national food security. Using genetic engineering technology to improve rice yield under abiotic stress is an effective way superior to conventional breeding methods. At present, regulatory genes and functional genes have been confirmed to enhance rice yield under abiotic stresses. This paper systematically reviewed the research progress of these genes in improving rice yield under drought, salt, low temperature, high temperature and other single and combined stresses, and analyzed the existing problems, so as to provide reference for rice variety breeding for stress tolerance and high yield.

Key words: rice, abiotic stress, genetic engineering, regulatory gene, function genes, yield

摘要：

干旱、盐、低温、高温等非生物胁迫严重影响水稻的生长发育及产量，提高非生物胁迫下水稻产量对保障国家粮食安全具有重要的现实意义。利用基因工程技术提高非生物胁迫下水稻产量是优于传统育种的有效途径。目前，已证实的可提高非生物胁迫下水稻产量的基因主要有调节基因和功能基因。文章综述了这些基因提高干旱、盐、低温、高温等单一胁迫及复合胁迫条件下水稻产量的研究进展，并分析了存在的问题，以期为水稻抗逆、高产育种提供参考。

关键词: 水稻, 非生物胁迫, 基因工程, 调节基因, 功能基因, 产量

CLC Number:

S511

DUAN Junzhi, YANG Cuiping, WANG Nan, QI Xueli, FENG Lili, YAN Zhaoling, QI Hongzhi, CHEN Haiyan, ZHANG Huifang, ZHUO Wenfei, LI Ying. Progress on Improving Rice Yield under Abiotic Stress by Genetic Engineering[J]. China Rice, 2023, 29(3): 15-23.

段俊枝, 杨翠萍, 王楠, 齐学礼, 冯丽丽, 燕照玲, 齐红志, 陈海燕, 张会芳, 卓文飞, 李莹. 利用基因工程技术提高非生物胁迫下水稻产量的研究进展[J]. 中国稻米, 2023, 29(3): 15-23.

References 61

[1]	ZHAO C, LIU B, PIAO S L, et al. Temperature increase reduces global yields of major crops in four independent estimates[J]. Proceedings of the National Academy of Sciences of the United States of America, 2017, 114: 9 326-9 331.
[2]	RAZA A, RAZZAQ A, MEHMOOD S S, et al. Impact of climate change on crops adaptation and strategies to tackle its outcome: A review[J]. Plants, 2019, doi: 10.3390/plants8020034.
[3]	GAO Y, WU M Q, ZHANG M J, et al. A maize phytochrome-interacting factors protein ZmPIF1 enhances drought tolerance by inducing stomatal closure and improves grain yield in Oryza sativa[J]. Plant Biotechnology Journal, 2018, 16(7): 1 375-1 387.
[4]	CHEN X L, JIANG L R, ZHENG J S, et al. A missense mutation in Large Grain Size 1 increases grain size and enhances cold tolerance in rice[J]. Journal of Experimental Botany, 2019, 70(15): 3 851-3 866.
[5]	ZENG Y, WEN J, ZHAO W, et al. Rational improvement of rice yield and cold tolerance by editing the three genes OsPIN5b, GS3, and OsMYB30 with the CRISPR-Cas9 system[J]. Frontiers in Plant Science, 2020, doi: 10.3389/fpls.2019.01663.
[6]	CHOI J, LEE W, AN G, et al. OsCBE1, a substrate receptor of cullin4-based E3 ubiquitin ligase, functions as a regulator of abiotic stress response and productivity in rice[J]. International Journal of Molecular Sciences, 2021, doi: 10.3390/ijms22052487.
[7]	PARK S I, KIM J J, KIM H S, et al. Enhanced glutathione content improves lateral root development and grain yield in rice plants[J]. Plant Molecular Biology, 2021, 105(4-5): 365-383.
[8]	PARK S I, KIM Y S, KIM J J, et al. Improved stress tolerance and productivity in transgenic rice plants constitutively expressing the Oryza sativa glutathione synthetase OsGS under paddy field conditions[J]. Journal of Plant Physiology, 2017, 215: 39-47.
[9]	LEE K, BACK K. Overexpression of rice serotonin N-acetyltransferase 1 in transgenic rice plants confers resistance to cadmium and senescence and increases grain yield[J]. Journal of Pineal Research, 2017, doi: 10.1111/jpi.12392.
[10]	WANG P, XU X, TANG Z, et al. OsWRKY28 regulates phosphate and arsenate accumulation, root system architecture and fertility in rice[J]. Frontiers in Plant Science, 2018, doi: 10.3389/fpls.2018.01330.
[11]	ZENG Z M, XIONG F J, YU X H, et al. Overexpression of a glyoxalase gene, OsGly I, improves abiotic stress tolerance and grain yield in rice (Oryza sativa L.)[J]. Plant Physiology and Biochemistry, 2016, 109: 62-71.
[12]	LO S F, CHENG M L, HSING Y C, et al. Rice Big Grain 1 promotes cell division to enhance organ development, stress tolerance and grain yield[J]. Plant Biotechnology Journal, 2020, 18(9): 1 969-1 983.
[13]	KANG J F, LI J M, GAO S, et al. Overexpression of the leucine-rich receptor-like kinase gene LRK2 increases drought tolerance and tiller number in rice[J]. Plant Biotechnology Journal, 2017, 15(9): 1 175-1 185.
[14]	FANG Y J, LIAO K F, DU H, et al. A stress-responsive NAC transcription factor SNAC3 confers heat and drought tolerance throughmodulation of reactive oxygen species in rice[J]. Journal of Experimental Botany, 2015, 66(21): 6 803-6 817.
[15]	JIN Y, PAN W Y, ZHENG X F, et al. OsERF101, an ERF family transcription factor, regulates drought stress response in reproductive tissues[J]. Plant Molecular Biology, 2018, 98(1-2): 51-65. PMID
[16]	GAO Y, WU M Q, ZHANG M J, et al. Roles of a maize phytochrome-interacting factors protein ZmPIF3 in regulation of drought stress responses by controlling stomatal closure in transgenic rice without yield penalty[J]. Plant Molecular Biology, 2018, 97(4-5): 311-323. PMID
[17]	TIAN P, LIU J F, MOU C L, et al. GW5-Like, a homolog of GW5, negatively regulates grain width, weight and salt resistance in rice[J]. Journal of Integrative Plant Biology, 2019, 61(11): 1 171-1 185.
[18]	VISHAL B, KRISHNAMURTHY P, RAMAMOORTHY R, et al. OsTPS8 controls yield-related traits and confers salt stress tolerance in rice by enhancing suberin deposition[J]. New Phytologist, 2019, 221(3): 1 369-1 386.
[19]	YIN W C, XIAO Y H, NIU M, et al. ARGONAUTE2 enhances grain length and salt tolerance by activating BIG GRAIN3 to modulate cytokinin distribution in rice[J]. The Plant Cell, 2020, 32(7): 2 292-2 306.
[20]	DONG N Q, SUN Y W, GUO T, et al. UDP-glucosyltransferase regulates grain size and abiotic stress tolerance associated with metabolic flux redirection in rice[J]. Nature Communications, 2020, doi: 10.1038/s41467-020-16403-5.
[21]	SELVARAJ M G, ISHIZAKI T, VALENCIA M, et al. Overexpression of an Arabidopsis thaliana galactinol synthase gene improves drought tolerance in transgenic rice and increased grain yield in the field[J]. Plant Biotechnology Journal, 2017, 15(11): 1 465-1 477.
[22]	BAKSHI A, MOIN M, KUMAR M U, et al. Ectopic expression of Arabidopsis Target of Rapamycin (AtTOR) improves water-use efficiency and yield potential in rice[J]. Scientific Reports, 2017, doi: 10.1038/srep42835.
[23]	CHEN J G, QI T T, HU Z, et al. OsNAR2.1 positively regulates drought tolerance and grain yield under drought stress conditions in rice[J]. Frontiers in Plant Science, 2019, doi: 10.3389/fpls.2019.00197.
[24]	USMAN B, NAWAZ G, ZHAO N, et al. 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[J]. International Journal of Molecular Sciences, 2020, doi: 10.3390/ijms21217854.
[25]	DEY A, SAMANTA M K, GAYEN S, et al. The sucrose non-fermenting 1-related kinase 2 gene SAPK9 improves drought tolerance and grain yield in rice by modulating cellular osmotic potential, stomatal closure and stress-responsive gene expression[J]. BMC Plant Biology, 2016, doi: 10.1186/s12870-016-0845-x.
[26]	LOU D J, CHEN Z, YU D Q, et al. SAPK2 contributes to rice yield by modulating nitrogen metabolic processes under reproductive stage drought stress[J]. Rice, 2020, doi: 10.1186/s12284-020-00395-3.
[27]	CHEN X, WANG Y F, L B, et al. The NAC family transcription factor OsNAP confers abiotic stress response throughthe ABA pathway[J]. Plant and Cell Physiology, 2014, 55(3): 604-619.
[28]	SHEN J B, LV B, LUO L Q, et al. The NAC-type transcription factor OsNAC2 regulates ABA-dependent genes and abiotic stress tolerance in rice[J]. Scientific Reports, 2017, doi: 10.1038/srep40641.
[29]	HU H H, DAI M Q, YAO J L, et al. Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice[J]. Proceedings of the National Academy of Sciences of the United States of America, 2006, 103(35): 12 987-12 992.
[30]	REDILLAS C, JEONG J S, KIM Y S, et al. The overexpression of OsNAC9 alters the root architecture of rice plants enhancing drought resistance and grain yield under field conditions[J]. Plant Biotechnology Journal, 2012, 10(7): 792-805.
[31]	JEONG J S, KIM Y S, BAEK K H, et al. Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under fielddrought conditions[J]. Plant Physiology, 2010, 153(1): 185-197.
[32]	JEONG J S, KIM Y S, REDILLAS M C, et al. OsNAC5 overexpression enlarges root diameter in rice plants leading to enhanced drought tolerance and increased grain yield in the field[J]. Plant Biotechnology Journal, 2013, 11(1): 101-114.
[33]	LEE D K, CHUNG P J, JEONG J S, et al. The rice OsNAC6 transcription factor orchestrates multiple molecular mechanisms involving root structural adaptions and nicotianamine biosynthesis for drought tolerance[J]. Plant Biotechnology Journal, 2017, 15(6): 754-764.
[34]	OH S J, KIM Y S, KWON C W, et al. Overexpression of the transcription factor AP37 in rice improves grain yieldunder drought conditions[J]. Plant Physiology, 2009, 150: 1 368-1 379.
[35]	JUNG H, CHUNG P J, PARK S, et al. Overexpression of OsERF48 causes regulation of OsCML16, a calmodulin-like protein gene that enhances root growth and drought tolerance[J]. Plant Biotechnology Journal, 2017, 15(10): 1 295-1 308.
[36]	XU W Y, TANG W S, WANG C X, et al. SiMYB56 confers drought stress tolerance in transgenic rice by regulating lignin biosynthesis and ABA signaling pathway[J]. Frontiers in Plant Science, 2020, doi: 10.3389/fpls.2020.00785.
[37]	CHEN Y S, HO T D, LIU L, et al. Sugar starvation-regulated MYBS2 and 14-3-3 protein interactions enhance plant growth, stress tolerance, and grain weight in rice[J]. Proceedings of The National Academy of Sciences of The United States of America, 2019, 116(43): 21 925-21 935.
[38]	DEY A, SAMANTA M K, GAYEN S, et al. Enhanced gene expression rather than natural polymorphism in coding sequence of the OsbZIP23 determines drought tolerance and yield improvement in rice genotypes[J]. PLoS One, 2016, doi: 10.1371/journal.pone.0150763.
[39]	CHANG Y, NGUYEN B H, XIE Y J, et al. Co-overexpression of the constitutively active form of OsbZIP46 and ABA-activated protein kinase SAPK6 improves drought and temperature stress resistance in rice[J]. Frontiers in Plant Science, 2017, doi: 10.3389/fpls.2017.01102.
[40]	Chander S, Almeida D M, Serra T S, et al. OsICE1 transcription factor improves photosynthetic performance and reduces grain losses in rice plants subjected to drought[J]. Environmental and Experimental Botany, 2 018, 150: 88-98.
[41]	PARK S I, KIM J J, SHIN S Y, et al. ASR enhances environmental stress tolerance and improves grain yield by modulating stomatal closure in rice[J]. Frontiers in Plant Science, 2020, doi: 10.3389/fpls.2019.01752.
[42]	SELVARAJ M G, JAN A, ISHIZAKI T, et al. Expression of the CCCH-tandem zinc finger protein gene OsTZF5 under a stress-inducible promoter mitigates the effect of drought stress on rice grain yield under field conditions[J]. Plant Biotechnology Journal, 2020, 18(8): 1 711-1 721.
[43]	NUTAN K K, SINGLA-PAREEK S L, PAREEK A. The Saltol QTL-localized transcription factor OsGATA8 plays an important role in stress tolerance and seed development in Arabidopsis and rice[J]. Journal of Experimental Botany, 2020, 71(2): 684-698.
[44]	XU C, LUO M, SUN X, et al. SiMYB19 from foxtail millet (Setaria italica) confers transgenic rice tolerance to high salt stress in the field[J]. International Journal of Molecular Sciences, 2022, doi: 10.3390/ijms23020756.
[45]	ALFATIH A, WU J, JAN S U, et al. Loss of rice PARAQUAT TOLERANCE 3 confers enhanced resistance to abiotic stresses and increases grain yield in field[J]. Plant, Cell & Environment, 2020, 43(11): 2 743-2 754.
[46]	TIAN Q X, SHEN L K, LUAN J X, et al. Rice shaker potassium channel OsAKT2 positively regulates salt tolerance and grain yield by mediating K⁺ redistribution[J]. Plant, Cell & Environment, 2021, 44(9): 2 951-2 965.
[47]	LIU C T, SCHLPPI M R, MAO B G, et al. The bZIP73 transcription factor controls rice cold tolerance at the reproductive stage[J]. Plant Biotechnology Journal, 2019, 17(9): 1 834-1 849.
[48]	XU Y, WANG R, WANG Y, et al. A point mutation in LTT1 enhances cold tolerance at the booting stage in rice[J]. Plant, Cell & Environment, 2020, 43(4): 992-1007.
[49]	EL-KEREAMY A, BI Y M, RANATHUNGE K, et al. The rice R2R3-MYB transcription factor OsMYB55 is involved in the tolerance to high temperature and modulates amino acid metabolism[J]. PLoS One, 2012, doi: 10.1371/journal.pone.0052030.
[50]	TANG Y T, LI X, LU W, et al. Enhanced photorespiration in transgenic rice over-expressing maize C₄ phosphoenolpyruvate carboxylase gene contributes to alleviating low nitrogen stress[J]. Plant Physiology and Biochemistry, 2018, 130: 577-588.
[51]	ACHARY V M M, SHERI V, MANNA M, et al. Overexpression of improved EPSPS gene results in field level glyphosate tolerance and higher grain yield in rice[J]. Plant Biotechnology Journal, 2020, 18(12): 2 504-2 519.
[52]	GUDDIMALLI R, SOMANABOINA A K, PALLE S R, et al. Overexpression of RNA-binding bacterial chaperones in rice leads to stay-green phenotype, improved yield and tolerance to salt and drought stresses[J]. Plant Physiology, 2021, 173(4): 1 351-1 368.
[53]	EL-ESAWI M A, ALAYAFI A A. Overexpression of rice Rab7 gene improves drought and heat tolerance and increases grain yield in rice (Oryza sativa L.)[J]. Genes, 2019, doi: 10.3390/genes10010056.
[54]	WANG C G, WANG G K, GAO Y, et al. A cytokinin-activation enzyme-like gene improves grain yield under various field conditions in rice[J]. Plant Molecular Biology, 2020, 102: 373-388. PMID
[55]	SODA N, GUPTA B K, ANWAR K, et al. Rice intermediate filament, OsIF, stabilizes photosynthetic machinery and yield under salinity and heat stress[J]. Scientific Reports, 2019, doi: 10.1038/s41598-018-22131-0.
[56]	ZENG Y, LI Q, WANG H Y, et al. Two NHX-type transporters from Helianthus tuberosus improve the tolerance of rice to salinity and nutrient deficiency stress[J]. Plant Biotechnology Journal, 2018, 16(1): 310-321.
[57]	JOSHI R, SAHOO K K, SINGH A K, et al. Enhancing trehalose biosynthesis improves yield potential in marker-free transgenic rice under drought, saline, and sodic conditions[J]. Journal of Experimental Botany, 2020, 71(2): 653-668. PMID
[58]	VERMA R K, KUMAR V V S, YADAV S K, et al. Overexpression of Arabidopsis ICE1 enhances yield and multiple abiotic stress tolerance in indica rice[J]. Plant Signaling & Behavior, 2020, doi: 10.1080/15592324.2020.1814547.
[59]	SENGUPTA S, MUKHERJEE S, BASAK P, et al. Significance of galactinol and raffinose family oligosaccharide synthesis in plants[J]. Frontiers in Plant Science, 2015, doi: 10.3389/fpls.2015.00656.
[60]	LIU X Q, HUANG D M, TAO J Y, et al. Identification and functional assay of the interaction motifs in the partner protein OsNAR2.1 of the two-component system for high-affinity nitrate transport[J]. New Phytologist, 2014, 204: 74-80. PMID
[61]	UMEZAWA T, YOSHIDA R, MARUYAMA K, et al. SRK2C, a SNF1-related protein kinase 2, improves drought tolerance by controlling stress-responsive gene expression in Arabidopsis thaliana[J]. Proceedings of the National Academy of Sciences of the United States of America, 2004, 101(49): 17 306-1 7311.