Abstract
Drought is one of the major abiotic stresses affecting the maize production worldwide. As a cross-pollination crop, maize is sensitive to water stress at flowering stage. Drought at this stage leads to asynchronous development of male and female flower organ and increased interval between anthesis and silking, which finally causes failure of pollination and grain yield loss. In the present study, the expansin gene ZmEXPA5 was cloned and its function in drought tolerance was characterized. An indel variant in promoter of ZmEXPA5 is significantly associated with natural variation in drought-induced anthesis-silking interval. The drought susceptible haplotypes showed lower expression level of ZmEXPA5 than tolerant haplotypes and lost the cis-regulatory activity of ZmDOF29. Increasing ZmEXPA5 expression in transgenic maize decreases anthesis-silking interval and improves grain yield under both drought and well-watered environments. In addition, the expression pattern of ZmEXPA5 was analyzed. These findings provide insights into the genetic basis of drought tolerance and a promising gene for drought improvement in maize breeding.
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References
Abbasi A, Malekpour M, Sobhanverdi S (2021) The Arabidopsis expansin gene (AtEXPA18) is capable to ameliorate drought stress tolerance in transgenic tobacco plants. Mol Biol Rep 48(8):5913–5922. https://doi.org/10.1007/s11033-021-06589-2
Alexander DH, Novembre J, Lange K (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19(9):1655–1664. https://doi.org/10.1101/gr.094052.109
Bradbury PJ, Zhang ZW, Kroon DE et al (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23(19):2633–2635. https://doi.org/10.1093/bioinformatics/btm308
Bruce WB, Edmeades GO, Barker TC (2002) Molecular and physiological approaches to maize improvement for drought tolerance. J Exp Bot 53(366):13–25. https://doi.org/10.1093/jexbot/53.366.13
Calderini DF, Castillo FM, Arenas MA et al (2021) Overcoming the trade-off between grain weight and number in wheat by the ectopic expression of expansin in developing seeds leads to increased yield potential. New Phytol 230(2):629–640. https://doi.org/10.1111/nph.17048
Chen LJ, Zou WS, Fei CY et al (2018) α-Expansin EXPA4 positively regulates abiotic stress tolerance but negatively regulates pathogen resistance in Nicotiana tabacum. Plant Cell Physiol 59(11):2317–2330. https://doi.org/10.1093/pcp/pcy155
Chen SK, Luo YX, Wang GJ et al (2020) Genome-wide identification of expansin genes in Brachypodium distachyon and functional characterization of BdEXPA27. Plant Sci 296:110490. https://doi.org/10.1016/j.plantsci.2020.110490
Cosgrove DJ (2021) Expanding wheat yields with expansin. New Phytol 230(2):403–405. https://doi.org/10.1111/nph.17245
Dal Santo S, Vannozzi A, Tornielli GB et al (2013) Genome-wide analysis of the expansin gene superfamily reveals grapevine-specific structural and functional characteristics. PLoS ONE 8(4):e62206. https://doi.org/10.1371/journal.pone.0062206
Feng XJ, Jia L, Cai YT et al (2022) ABA-inducible DEEPER ROOTING 1 improves adaptation of maize to water deficiency. Plant Biotechnol J 20(11):2077–2088. https://doi.org/10.1111/pbi.13889
Gao HJ, Cui JJ, Liu SX et al (2022) Natural variations of ZmSRO1d modulate the trade-off between drought resistance and yield by affecting ZmRBOHC-mediated stomatal ROS production in maize. Mol Plant 15(10):1558–1574. https://doi.org/10.1016/j.molp.2022.08.009
Godfray HCJ, Beddington JR, Crute IR et al (2010) Food security: the challenge of feeding 9 billion people. Science 327(5967):812–818. https://doi.org/10.1126/science.1185383
Gupta A, Rico-Medina A, Cano-Delgado AI (2020) The physiology of plant responses to drought. Science 368(6488):266–269. https://doi.org/10.1126/science.aaz7614
Han LQ, Zhong WS, Qian J et al (2023) A multi-omics integrative network map of maize. Nat Genet 55(1):144–153. https://doi.org/10.1038/s41588-022-01262-1
Hao LY, Liu XY, Zhang XJ et al (2020) Genome-wide identification and comparative analysis of drought related genes in roots of two maize inbred lines with contrasting drought tolerance by RNA sequencing. J Integr Agri 19(2):449–464. https://doi.org/10.1016/S2095-3119(19)62660-2
Hepler NK, Bowman A, Carey RE et al (2020) Expansin gene loss is a common occurrence during adaptation to an aquatic environment. Plant J 101(3):666–680. https://doi.org/10.1111/tpj.14572
Li C, Guan H, Jing X et al (2022b) Genomic insights into historical improvement of heterotic groups during modern hybrid maize breeding. Nat Plants 8(7):750–763. https://doi.org/10.1038/s41477-022-01190-2
Li XD, Gao YQ, Wu WH et al (2022a) Two calcium-dependent protein kinases enhance maize drought tolerance by activating anion channel ZmSLAC1 in guard cells. Plant Biotechnol J 20(1):143–157. https://doi.org/10.1111/pbi.13701
Liu BX, Zhang B, Yang ZR et al (2021a) Manipulating ZmEXPA4 expression ameliorates the drought-induced prolonged anthesis and silking interval in maize. Plant Cell 33(6):2058–2071. https://doi.org/10.1093/plcell/koab083
Liu WM, Xu LA, Lin H et al (2021b) Two expansin genes, AtEXPA4 and AtEXPB5, are redundantly required for pollen tube growth and AtEXPA4 is involved in primary root elongation in Arabidopsis thaliana. Genes 12(2):249. https://doi.org/10.3390/genes12020249
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262
Lobell DB, Roberts MJ, Schlenker W et al (2014) Greater sensitivity to drought accompanies maize yield increase in the US Midwest. Science 344(6183):516–519. https://doi.org/10.1126/science.1251423
Lu PT, Kang M, Jiang XQ et al (2013) RhEXPA4, a rose expansin gene, modulates leaf growth and confers drought and salt tolerance to Arabidopsis. Planta 237(6):1547–1559. https://doi.org/10.1007/s00425-013-1867-3
Mao HD, Wang HW, Liu SX et al (2015) A transposable element in a NAC gene is associated with drought tolerance in maize seedlings. Nat Commun 6:8326. https://doi.org/10.1038/ncomms9326
Mayorga-Gomez A, Nambeesan SU (2020) Temporal expression patterns of fruit-specific α-EXPANSINS during cell expansion in bell pepper (Capsicum annuum L.). BMC Plant Biol 20(1):241. https://doi.org/10.1186/s12870-020-02452-x
McQueen-Mason SJ, Durachko DM, Cosgrove DJ (1992) Two endogenous proteins that induce cell wall extension in plants. Plant Cell 4(11):1425–1433. https://doi.org/10.1105/tpc.4.11.1425
Narayan JA, Chakravarthi M, Nerkar G et al (2021) Overexpression of expansin EaEXPA1, a cell wall loosening protein enhances drought tolerance in sugarcane. Ind Crops Prod 159:113035. https://doi.org/10.1016/j.indcrop.2020.113035
Sampedro J, Carey RE, Cosgrove DJ (2006) Genome histories clarify evolution of the expansin superfamily: new insights from the poplar genome and pine ESTs. J Plant Res 119(1):11–21. https://doi.org/10.1007/s10265-005-0253-z
Sampedro J, Lee Y, Carey RE et al (2005) Use of genomic history to improve phylogeny and understanding of births and deaths in a gene family. Plant J 44(3):409–419. https://doi.org/10.1111/j.1365-313X.2005.02540.x
Sun XP, Xiang YL, Dou NN et al (2023) The role of transposon inverted repeats in balancing drought tolerance and yield-related traits in maize. Nat Biotechnol 41:120–127. https://doi.org/10.1038/s41587-022-01470-4
Tian T, Wang SH, Yang SP et al (2023) Genome assembly and genetic dissection of a prominent drought-resistant maize germplasm. Nat Genet 55:496–506. https://doi.org/10.1038/s41588-023-01297-y
Tuberosa R, Salvi S, Sanguineti MC et al (2002) Mapping QTLs regulating morpho-physiological traits and yield: case studies, shortcomings and perspectives in drought-stressed maize. Ann Bot 89:941–963. https://doi.org/10.1093/aob/mcf134
Walley JW, Sartor RC, Shen ZX et al (2016) Integration of omic networks in a developmental atlas of maize. Science 353(6301):814–818. https://doi.org/10.1126/science.aag1125
Wang XL, Wang HW, Liu SX et al (2016) Genetic variation in ZmVPP1 contributes to drought tolerance in maize seedlings. Nat Genet 48(10):1233–1241. https://doi.org/10.1038/ng.3636
Wu X, Fen H, Wu D et al (2021) Using high-throughput multiple optical phenotyping to decipher the genetic architecture of maize drought tolerance. Genome Biol 22(1):185. https://doi.org/10.1186/s13059-021-02377-0
Yang JJ, Zhang GQ, An J et al (2020) Expansin gene TaEXPA2 positively regulates drought tolerance in transgenic wheat (Triticum aestivum L.). Plant Sci 298:110596. https://doi.org/10.1016/j.plantsci.2020.110596
Yang WN, Guo ZL, Huang CL et al (2014) Combining high-throughput phenotyping and genome-wide association studies to reveal natural genetic variation in rice. Nat Commun 5:5087. https://doi.org/10.1038/ncomms6087
Zhang BY, Chang L, Sun WN et al (2021b) Overexpression of an expansin-like gene, GhEXLB2 enhanced drought tolerance in cotton. Plant Physiol Biochem 162:468–475. https://doi.org/10.1016/j.plaphy.2021.03.018
Zhang F, Wu JF, Sade N et al (2021a) Genomic basis underlying the metabolome-mediated drought adaptation of maize. Genome Biol 22(1):260. https://doi.org/10.1186/s13059-021-02481-1
Zhang W, Yan HW, Chen WJ et al (2014) Genome-wide identification and characterization of maize expansin genes expressed in endosperm. Mol Genet Genomics 289(6):1061–1074. https://doi.org/10.1007/s00438-014-0867-8
Zhang XJ, Liu XY, Zhang DF et al (2017) Genome-wide identification of gene expression in contrasting maize inbred lines under field drought conditions reveals the significance of transcription factors in drought tolerance. PLoS ONE 12(7):e0179477. https://doi.org/10.1371/journal.pone.0179477
Zhu Y, Wu NN, Song WL et al (2014) Soybean (Glycine max) expansin gene superfamily origins: segmental and tandem duplication events followed by divergent selection among subfamilies. BMC Plant Biol 14:93. https://doi.org/10.1186/1471-2229-14-93
Zhu ZH, Zhang FT, Hu H et al (2016) Integration of summary data from GWAS and eQTL studies predicts complex trait gene targets. Nat Genet 48(5):481–487. https://doi.org/10.1038/ng.3538
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This research was supported by the national key research and development program of China (2021YFD1200705, 2016YFD0101803, and 2017YFD0300405).
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XL, YL, YL, and TW conceived and designed the experiment. KT, YL, and YH performed most of the experiments and analyzed the data. YL, DZ, CL, GH, YS, and YS carried out the field experiment. KT, YH, YL, and XL wrote and edited the manuscript.
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Tao, K., Li, Y., Hu, Y. et al. Overexpression of ZmEXPA5 reduces anthesis-silking interval and increases grain yield under drought and well-watered conditions in maize. Mol Breeding 43, 84 (2023). https://doi.org/10.1007/s11032-023-01432-x
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DOI: https://doi.org/10.1007/s11032-023-01432-x