Maize leaves drought-responsive genes revealed by comparative transcriptome of two cultivars during the filling stage

Autoři: Hongyu Jin aff001;  Songtao Liu aff001;  Tinashe Zenda aff001;  Xuan Wang aff001;  Guo Liu aff001;  Huijun Duan aff001
Působiště autorů: Department of Crop Genetics and Breeding, College of Agronomy, Hebei Agricultural University, Baoding, China aff001;  North China Key Laboratory for Crop Germplasm Resources of the Education Ministry, Hebei Agricultural University, Baoding, China aff002
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0223786


Like other important cereal crop in modern agricultural production, maize is also threatened by drought. And the drought stress during maize filling stage will directly affect the quality (protein or oil concentration) and also the weight of grain. Therefore, different from previous studies focusing on inbred lines and pot experiment at seedling stage, current study selected filling stage of the adult plant and planting maize in the experimental field. Two hybrids cultivars with different drought tolerant were used for drought and water treatment respectively. We performed transcriptome sequencing analysis of 4 groups, 12 samples, and obtained 651.08 million raw reads. Then the data were further processed by mapping to a reference genome, GO annotation, enrichment analysis and so on. Among them we focus on the different change trends of water treatment and drought treatment, and the different responses of two drought-tolerant cultivars to drought treatment. Through the analysis, several transcripts which encode nitrogen metabolic, protein phosphorylation, MYB,AP2/ERF, HB transcriptional factor, O-glycosyl hydrolases and organic acid metabolic process were implicated with maize drought stress. Our data will offer insights of the identification of genes involved in maize drought stress tolerance, which provides a theoretical basis for maize drought resistance breeding.

Klíčová slova:

Cereal crops – Drought adaptation – Gene expression – Gene regulation – Maize – Metabolic processes – Plant resistance to abiotic stress – Water resources


1. Campos H, Cooper A, Habben JE, Edmeades GO, Schussler JR. Improving drought tolerance in maize: a view from industry. Field Crops Research. 2004;90(1):19–34. doi: 10.1016/j.fcr.2004.07.003

2. Li GK, Gao J, Peng H, Shen YO, Ding HP, Zhang ZM, et al. Proteomic changes in maize as a response to heavy metal (lead) stress revealed by iTRAQ quantitative proteomics. Genetics and Molecular Research. 2016;15(1). doi: 10.4238/gmr.15017254 26909923

3. Min H, Chen C, Wei S, Shang X, Sun M, Xia R, et al. Identification of Drought Tolerant Mechanisms in Maize Seedlings Based on Transcriptome Analysis of Recombination Inbred Lines. Frontiers in Plant Science. 2016;7. doi: 10.3389/fpls.2016.01080 27507977

4. Zdenek Z, Petr H, Karel P, Daniela S, Jan B, Miroslav T. Impacts of water availability and drought on maize yield—A comparison of 16 indicators. Agricultural Water Management. 2017;188:126–35. doi: 10.1016/j.agwat.2017.04.007

5. Rurinda J, van Wijk MT, Mapfumo P, Descheemaeker K, Supit I, Giller KE. Climate change and maize yield in southern Africa: what can farm management do? Global Change Biology. 2015;21(12):4588–601. doi: 10.1111/gcb.13061 26251975

6. Ghatak A, Chaturvedi P, Weckwerth W. Cereal Crop Proteomics: Systemic Analysis of Crop Drought stress Responses Towards Marker-Assisted Selection Breeding. Frontiers in Plant Science. 2017;8. doi: 10.3389/fpls.2017.00757 28626463

7. Miao Z, Han Z, Zhang T, Chen S, Ma C. A systems approach to a spatio-temporal understanding of the drought stress response in maize. Scientific Reports. 2017;7. doi: 10.1038/s41598-017-06929-y 28747711

8. V A. Introductory chapter: climate changes and abiotic stress in plants. IntechOpen. 2018.

9. Zheng J, Fu J, Gou M, Huai J, Liu Y, Jian M, et al. Genome-wide transcriptome analysis of two maize inbred lines under drought stress. Plant Molecular Biology. 2010;72(4–5):407–21. doi: 10.1007/s11103-009-9579-6 19953304

10. Jurgens SK, Johnson RR, Boyer JS. Dry Matter Production and Translocation in Maize Subjected to Drought during Grain Fill. Agronomy Journal. 1978;70(4):678–82.

11. Wang Z, Xu Y, Chen T, Zhang H, Yang J, Zhang J. Abscisic acid and the key enzymes and genes in sucrose-to-starch conversion in rice spikelets in response to soil drying during grain filling. Planta. 2015;241(5):1091–107. doi: 10.1007/s00425-015-2245-0 25589060

12. Zhang L, Liang XG, Shen S, Yin H, Zhou LL, Gao Z, et al. Increasing the abscisic acid level in maize grains induces precocious maturation by accelerating grain filling and dehydration. Plant Growth Regulation. 2018;86(1):65–79.

13. Ghorbani A, Izadpanah K, Dietzgen RG. Changes in maize transcriptome in response to maize Iranian mosaic virus infection. Plos One. 2018;13(4). doi: 10.1371/journal.pone.0194592 29634778

14. Miao Z, Han Z, Zhang T, Chen S, Ma C. A systems approach to a spatio-temporal understanding of the drought stress response in maize. Sci Rep. 2017;7(1).

15. Jogaiah S, Govind SR, Lam-Son Phan T. Systems biology-based approaches toward understanding drought tolerance in food crops. Critical Reviews in Biotechnology. 2013;33(1):23–39. doi: 10.3109/07388551.2012.659174 22364373

16. Luan M, Xu M, Lu Y, Zhang L, Fan Y, Wang L. Expression of zma-miR169 miRNAs and their target ZmNF-YA genes in response to abiotic stress in maize leaves. Gene. 2015;555(2):178–85. doi: 10.1016/j.gene.2014.11.001 25445264

17. Zhang L, Li X-H, Gao Z, Shen S, Liang X-G, Zhao X, et al. Regulation of maize kernel weight and carbohydrate metabolism by abscisic acid applied at the early and middle post-pollination stages in vitro. Journal of Plant Physiology. 2017;216:1–10. doi: 10.1016/j.jplph.2017.05.005 28544894

18. Oliver SN, Dennis ES, Dolferus R. ABA regulates apoplastic sugar transport and is a potential signal for cold-induced pollen sterility in rice. Plant and Cell Physiology. 2007;48(9):1319–30. doi: 10.1093/pcp/pcm100 17693452

19. Wang N, Li L, Gao W-w, Wu Y-b, Yong H-j, Weng J-f, et al. Transcriptomes of early developing tassels under drought stress reveal differential expression of genes related to drought tolerance in maize. Journal of Integrative Agriculture. 2018;17(6):1276–88. doi: 10.1016/s2095-3119(17)61777-5

20. Muraya MM, Schmutzer T, Ulpinnis C, Scholz U, Altmann T. Targeted Sequencing Reveals Large-Scale Sequence Polymorphism in Maize Candidate Genes for Biomass Production and Composition. Plos One. 2015;10(7). doi: 10.1371/journal.pone.0132120 26151830

21. Edmeades GO. Progress in Achieving and Delivering Drought Tolerance in Maize—An Update. ISAA: Ithaca. 2013.

22. Bhanu BD, Ulaganathan K, Shanker AK, Desai S. RNA-seq Analysis of Irrigated vs. Water Stressed Transcriptomes of Zea mays Cultivar Z59. Frontiers in Plant Science. 2016;7.

23. Zenda T, Liu S, Wang X, Liu G, Jin H, Dong A, et al. Key Maize Drought-Responsive Genes and Pathways Revealed by Comparative Transcriptome and Physiological Analyses of Contrasting Inbred Lines. International Journal of Molecular Sciences. 2019;20(6). doi: 10.3390/ijms20061268 30871211

24. Jimenez S, Dridi J, Gutierrez D, Moret D, Irigoyen JJ, Moreno MA, et al. Physiological, biochemical and molecular responses in four Prunus rootstocks submitted to drought stress. Tree Physiology. 2013;33(10):1061–75. doi: 10.1093/treephys/tpt074 24162335

25. Ksouri N, Jimenez S, Wells CE, Contreras-Moreira B, Gogorcena Y. Transcriptional Responses in Root and Leaf of Prunus persica under Drought Stress Using RNA Sequencing. Frontiers in Plant Science. 2016;7. doi: 10.3389/fpls.2016.01715 27933070

26. Zhang X, Lei L, Lai J, Zhao H, Song W. Effects of drought stress and water recovery on physiological responses and gene expression in maize seedlings. Bmc Plant Biology. 2018;18. doi: 10.1186/s12870-018-1281-x 29685101

27. Lam Dai V, Stes E, Van Bel M, Nelissen H, Maddelein D, Inze D, et al. Up-to-Date Workflow for Plant (Phospho)proteomics Identifies Differential Drought-Responsive Phosphorylation Events in Maize Leaves. Journal of Proteome Research. 2016;15(12):4304–17. doi: 10.1021/acs.jproteome.6b00348 27643528

28. Xu Juan, Zhang Shuqun. Mitogen-activated protein kinase cascades in signaling plant growth and development. Trends in Plant Science. 2015;20(1):56–64. doi: 10.1016/j.tplants.2014.10.001 25457109

29. Hu X, Li N, Wu L, Li C, Li C, Zhang L, et al. Quantitative iTRAQ-based proteomic analysis of phosphoproteins and ABA-regulated phosphoproteins in maize leaves under osmotic stress. Scientific Reports. 2015;5:15626. doi: 10.1038/srep15626 26503333

30. Sui Z, Niu L, Yue G, Yang A, Zhang J. Cloning and expression analysis of some genes involved in the phosphoinositide and phospholipid signaling pathways from maize (Zea mays L.). Gene. 2008;426(1):47–56.

31. Lu T, Yang Y, Yao B, Liu S, Zhou Y, Zhang C. Template-based structure prediction and classification of transcription factors in Arabidopsis thaliana. Protein Science. 2012;21(6):828–38. doi: 10.1002/pro.2066 22549903

32. Shikha M, Kanika A, Rao AR, Mallikarjuna MG, Gupta HS, Nepolean T. Genomic Selection for Drought Tolerance Using Genome-Wide SNPs in Maize. Frontiers in Plant Science. 2017;8. doi: 10.3389/fpls.2017.00550 28484471

33. Zhou M-L, Tang Y-X, Wu Y-M. Genome-Wide Analysis of AP2/ERF Transcription Factor Family in Zea Mays. Current Bioinformatics. 2012;7(3):324–32. doi: 10.2174/157489312802460776

34. ZINATI Z, NAZARI L, BAGNARESI P, RAVASH R. In silico identification of transcription factors associated with the biosynthesis of carotenoids in corn (Zea mays L.). BioTechnologia. 2017;98. doi: 10.5114/bta.2017.66616

35. Zhao Y, Cheng X, Liu X, Wu H, Bi H, Xu H. The Wheat MYB Transcription Factor TaMYB31 Is Involved in Drought Stress Responses in Arabidopsis. Frontiers in Plant Science. 2018;9. doi: 10.3389/fpls.2018.01426 30323824

36. Wang G, Weng L, Li M, Xiao H. Response of Gene Expression and Alternative Splicing to Distinct Growth Environments in Tomato. International Journal of Molecular Sciences. 2017;18(3). doi: 10.3390/ijms18030475 28257093

37. Pelleschi S, Leonardi A, Rocher JP, Cornic G, de Vienne D, Thevenot C, et al. Analysis of the relationships between growth, photosynthesis and carbohydrate metabolism using quantitative trait loci (QTLs) in young maize plants subjected to water deprivation. Molecular Breeding. 2006;17(1):21–39. doi: 10.1007/s11032-005-1031-2

38. Sicher R, Bunce J, Barnaby J, Bailey B. Water-deficiency effects on single leaf gas exchange and on C-4 pathway enzymes of maize genotypes with differing abiotic stress tolerance. Photosynthetica. 2015;53(1):3–10. doi: 10.1007/s11099-015-0074-9

39. Xin L, Zheng H, Yang Z, Guo J, Liu T, Sun L, et al. Physiological and proteomic analysis of maize seedling response to water deficiency stress. Journal of Plant Physiology. 2018;228:29–38. doi: 10.1016/j.jplph.2018.05.005 29852332

40. Bray EA. Genes commonly regulated by water-deficit stress in Arabidopsis thaliana. Journal of Experimental Botany. 2004;55(407):2331–41. doi: 10.1093/jxb/erh270 15448178

41. Opassiri R, Pomthong B, Onkoksoong T, Akiyama T, Esen A, Cairns JRK. Analysis of rice glycosyl hydrolase family 1 and expression of Os4bglu12 β-glucosidase. BMC Plant Biology,6,1(2006-12-29). 2006;6(1):33.

42. Li Y-j, Li P, Wang T, Zhang F-j, Huang X-x, Hou B-k. The maize secondary metabolism glycosyltransferase UFGT2 modifies flavonols and contributes to plant acclimation to abiotic stresses. Annals of Botany. 2018;122(7):1203–17. doi: 10.1093/aob/mcy123 29982479

43. Takashima S, Abe T, Yoshida S, Kawahigashi H, Saito T, Tsuji S, et al. Analysis of sialyltransferase-like proteins from Oryza sativa. Journal of Biochemistry. 2006;139(2):279–87. doi: 10.1093/jb/mvj029 16452316

44. Ma C, Li B, Wang L, Xu ML, Lizhu E, Jin H, et al. Characterization of phytohormone and transcriptome reprogramming profiles during maize early kernel development. 2019.

45. Liu Y, Fang Xa, Chen G, Ye Y, Xu J, Ouyang G, et al. Recent development in sample preparation techniques for plant hormone analysis. Trac-Trends in Analytical Chemistry. 2019;113:224–33. doi: 10.1016/j.trac.2019.02.006

46. Mahrokh A, Pour MN, Dezfuli HAR, Choukan R. Evaluation of Relationship Between Auxin and Cytokinine Hormones on Yield and Yield Components of Maize under Drought Stress Condition Pizhūhishhā-yi zirāī-i Īrān. 2016;14.

47. Tumova L, Tarkowska D, Rehorova K, Markova H, Kocova M, Rothova O, et al. Drought-tolerant and drought-sensitive genotypes of maize (Zea mays L.) differ in contents of endogenous brassinosteroids and their drought-induced changes. Plos One. 2018;13(5).

48. Lee J, Shim D, Moon S, Kim H, Bae W, Kim K, et al. Genome-wide transcriptomic analysis of BR-deficient Micro-Tom reveals correlations between drought stress tolerance and brassinosteroid signaling in tomato. Plant Physiology and Biochemistry. 2018;127:553–60. doi: 10.1016/j.plaphy.2018.04.031 29723826

49. Makarevitch I, Thompson A, Muehlbauer GJ, Springer NM. Brd1 Gene in Maize Encodes a Brassinosteroid C-6 Oxidase. Plos One. 2012;7(1). doi: 10.1371/journal.pone.0030798 22292043

50. Peiffer JA, Romay MC, Gore MA, Flint-Garcia SA, Zhang Z, Millard MJ, et al. The genetic architecture of maize height. Genetics. 2014;196(4):1337–56. doi: 10.1534/genetics.113.159152 24514905

51. Vallabhaneni R, Wurtzel ET. From epoxycarotenoids to ABA: The role of ABA 8′-hydroxylases in drought-stressed maize roots. Archives of Biochemistry & Biophysics. 2010;504(1):112–7.

52. Takeuchi J, Okamoto M, Mega R, Kanno Y, Ohnishi T, Seo M, et al. Abscinazole-E3M, a practical inhibitor of abscisic acid 8 '-hydroxylase for improving drought tolerance. Scientific Reports. 2016;6. doi: 10.1038/srep37060 27841331

53. Iuchi S, Kobayashi M, Taji T, Naramoto M, Seki M, Kato T, et al. Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant Journal. 2001;27(4):325–33. doi: 10.1046/j.1365-313x.2001.01096.x 11532178

54. Nitsch LMC, Oplaat C, Feron R, Ma Q, Wolters-Arts M, Hedden P, et al. Abscisic acid levels in tomato ovaries are regulated by LeNCED1 and SlCYP707A1. Planta. 2009;229(6):1335–46. doi: 10.1007/s00425-009-0913-7 19322584

55. Xu L-m, Liu C, Cui B-m, Wang N, Zhao Z, Zhou L-n, et al. Transcriptomic responses to aluminum (Al) stress in maize. Journal of Integrative Agriculture. 2018;17(9):1946–58. doi: 10.1016/s2095-3119(17)61832-x

56. Wang H, Bai B, Bai Z, Shi L, Ye J, Fan S, et al. Enzymatic regulation of organic acid metabolism in an alkali-tolerant halophyte Chloris virgata during response to salt and alkali stresses African Journal of Biotechnology. 2016;15. doi: 10.5897/AJB2016.15580

57. Ranieri A, Bernardi R, Lanese P, Soldatini GF. Changes in free amino acid content and protein pattern of maize seedlings under water stress. Environmental & Experimental Botany. 1989;29(3):351–7.

58. Zhang J, Li J, Garcia-Ruiz H, Bates PD, Mirkov TE, Wang X. A stearoyl-acyl carrier protein desaturase, NbSACPD-C, is critical for ovule development in Nicotiana benthamiana. Plant Journal. 2014;80(3):489–502. doi: 10.1111/tpj.12649 25155407

59. Zhang YM, Wang CC, Hu HH, Yang L. Cloning and expression of three fatty acid desaturase genes from cold-sensitive lima bean (Phaseolus lunatus L.). Biotechnology Letters. 2011;33(2):395–401. doi: 10.1007/s10529-010-0432-4 20953666

60. Kachroo P, Shanklin J, Shah J, Whittle EJ, Klessig DF. A fatty acid desaturase modulates the activation of defense signaling pathways in plants. Proceedings of the National Academy of Sciences of the United States of America. 2001;98(16):9448–53. doi: 10.1073/pnas.151258398 11481500

61. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods. 2001;25(4):402–8. doi: 10.1006/meth.2001.1262 11846609

Článek vyšel v časopise


2019 Číslo 10