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Characterization on the water deprivation-associated physiological traits as well as the related differential genes during seed filling stage in wheat (T. aestivum L.)

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Abstract

Improvement on water use efficiency of the plants contributes to the sustainable crop production worldwide. In this study, we reported the physiological and growth traits at late stage, transcriptome profiling during seed filling period, and the function of TaMPK16 (encoding mitogen-activated protein kinase 16), a drought-inducible gene in wheat plants, in mediating drought adaptation of plants upon water deprivation. Compared with those grown under normal condition, the plants underlying deficit irrigation displayed increased proline and soluble sugar contents whereas lowered plant biomass and grain yields in tested cultivars. Shimai 22, a drought-tolerant cultivar, exhibited improved osmolytes and improved agronomic traits under DI relative to Jimai 585, an affluent water-acclimated cultivar. A total of 1712 genes were differentially expressed (DE) in leaves of Shimai 22 under water deprivation condition; they were categorized into the functional groups of biological process, cellular components, and molecular function and concentrated into the GO terms of metabolic process, metal ion binding, oxidation–reduction process, and catalytic activity, involving major biochemical metabolisms of glyoxylate and dicarboxylate, pyruvate, starch and sucrose, and amino and nucleotide sugars. Transgene analysis on TaMAPK16, a significantly upregulated DE gene, confirmed its role in mediating plant drought tolerance; the lines with TaMAPK16 overexpression conferred plants enhanced biomass, osmolytes biosynthesis, antioxidant enzyme activities, and photosynthetic function. These results suggested that plant water-deficit response during seed filling stage is associated with drastically modified transcription of huge genes that are involved in diverse physiological processes. TaMPK16 can be acted as a valuable target for breeding drought-tolerant varieties of T. aestivum.

Key message

Quantities of differentially expressed genes categorized into diverse functional groups contribute plant growth and agronomic traits in wheat plants upon water deprivation, via modulation of various physiological and biochemical processes associated with plant water deficit adaptation.

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References

  1. Acuña TB, Lisson S, Johnson P et al (2017) Yield and water-use efficiency of wheat in a high-rainfall environment. Crop Pasture Sci 66:419–429

  2. Agarwal PK, Gupta K, Jha B (2010) Molecular characterization of the Salicornia brachiata SbMAPKK gene and its expression by abiotic stress. Mol Biol Rep 37:981–986

  3. Ali MA, Zulkiffal M, Anwar J et al (2015) Morpho-physiological diversity in advanced lines of bread wheat under drought conditions at post-anthesis stage. J Animal Plant Sci 25:431–441

  4. Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 9:1165–1188

  5. Boudsocq M, Willmann MR, McCormack M, Lee H, Shan L, He P, Bush J, Cheng SH, Sheen J (2010) Differential innate immune signalling via Ca(2+) sensor protein kinases. Nature 464:418–422

  6. Budak H, Kantar M, Yucebilgili Kurtoglu K (2013) Drought tolerance in modern and wild wheat. Sci World J 2013:548246

  7. Coca M, San SB (2010) AtCPK1 calcium-dependent protein kinase mediates pathogen resistance in Arabidopsis. Plant J 63:526–540

  8. Dai H, Jia G, Shan C (2015) Jasmonic acid-induced hydrogen peroxide activates MEK1/2 in upregulating the redox states of ascorbate and glutathione in wheat leaves. Acta Physiol Plant 37:200

  9. Das R, Pandey GK (2009) Expressional analysis and role of calcium regulated kinases in abiotic stress signaling. Curr Genom 11:2–13

  10. De Smet I, Voss U, Jürgens G, Beeckman T (2009) Receptor-like kinases shape the plant. Nat Cell Biol 11:1166–1173

  11. Dhanda SS, Sethi GS, Behl RK (2010) Indices of drought tolerance in wheat genotypes at early stages of plant growth. J Agron Crop Sci 190:6–12

  12. Du X, Zhao X, Liu X, Guo C, Lu W, Gu J, Xiao K (2013) Overexpression of TaSRK2C1, a wheat SNF1-related protein kinase gene, increases tolerance to dehydration, salt, and low temperature in transgenic tobacco. Plant Mol Biol Rep 31:810–821

  13. Garg B, Puranik S, Misra S et al (2013) Transcript profiling identifies novel transcripts with unknown functions as primary response components to osmotic stress in wheat (Triticum aestivum L.). Plant Cell Tissue Organ Cult 113:91–101

  14. Golldack D, Li C, Mohan H, Probst N (2014) Tolerance to drought and salt stress in plants: unraveling the signaling networks. Front Plant Sci 5:151

  15. Guo C, Zhao X, Liu X, Zhang L, Gu J, Li X et al (2013) Function of wheat phosphate transporter gene TaPHT2;1 in Pi translocation and plant growth regulation under replete and limited Pi supply conditions. Planta 237:1163–1178

  16. Guóth A, Benyó D, Csiszár J et al (2010) Relationship between osmotic stress-induced abscisic acid accumulation, biomass production and plant growth in drought-tolerant and -sensitive wheat cultivars. Acta Physiol Plant 32(4):719–727

  17. Medrano H, Tomás M, Martorell S et al (2015) From leaf to whole-plant water use efficiency(wue)in complex canopies: limitations of leaf wue as a selection target. Crop J 3:220–228

  18. Huang XS, Liu JH, Chen XJ (2010) Overexpression of PtrABF gene, a bZIP transcription factor isolated from Poncirus trifoliata, enhances dehydration and drought tolerance in tobacco via scavenging ROS and modulating expression of stress-responsive genes. BMC Plant Biol 10:230

  19. Huseynova IM (2012) Photosynthetic characteristics and enzymatic antioxidant capacity of leaves from wheat cultivars exposed to drought. Biochim Et Biophys Acta Bioenergy 1817:1516–1523

  20. Jonak C, Kiegerl S, Ligterink W et al (1996) Stress signaling in plants: a mitogen-activated protein kinase pathway is activated by cold and drought. Proc Natl Acad Sci USA 93:11274–11279

  21. Kang J, Li J, Shuang Gao C, Tian XZ (2017) Overexpression of the leucine-rich receptor-like kinase gene LRK2 increases drought tolerance and tiller number in rice. Plant Biotechnol J 15:1175–1185

  22. Kim D, Pertea G, Trapnell C, Kelley PR, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14:R36

  23. Křenek P, Niks RE, Vels A, Vyplelová P (2015) Genome-wide analysis of the barley MAPK gene family and its expression patterns in relation to Puccinia hordei infection. Acta Physiol Plant 37:254

  24. Krannich CT, Maletzki L, Kurowsky C, Horn R (2015) Network candidate genes in breeding for drought tolerant crops. Int J Mol Sci 16:16378–16400

  25. Kumar K, Rao KP, Sharma P, Sinha AK (2008) Differential regulation of rice mitogen activated protein kinase kinase (MKK) by abiotic stress. Plant Physiol Biochem 46:891–897

  26. Lim CW, Park C, Kim J-H, Joo H, Hong E, Lee SC (2017) Pepper CaREL1, a ubiquitin E3 ligase, regulates drought tolerance via the ABA-signalling pathway. Sci Rep 7:477

  27. Liu H, Sultan MA, Liu XL, Zhang J, Yu F, Zhao HX (2015) Physiological and comparative proteomic analysis reveals different drought responses in roots and leaves of drought-tolerant wild wheat (Triticum boeoticum). PLoS ONE 10(4):e0121852

  28. Moghaddam ME, Trethowan RM, William HM et al (2005) Assessment of genetic diversity in bread wheat genotypes for tolerance to drought using AFLPs and agronomic traits. Euphytica 141:147–156

  29. Mori IC et al (2006) CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca(2+)-permeable channels and stomatal closure. PLoS Biol 4:e327

  30. Morillo SA, Tax FE (2006) Functional analysis of receptor-like kinases in monocots and dicots. Curr Opin Plant Biol 9:460–469

  31. Munemasa S, Hossain MA, Nakamura Y, Mori IC, Murata Y (2011) The Arabidopsis calcium-dependent protein kinase, CPK6, functions as a positive regulator of methyl jasmonate signaling in guard cells. Plant Physiol 155:553–561

  32. Nakagami H, Kiegerl S, Hirt H (2004) OMTK1, a novel MAPKKK, channels oxidative stress signaling through direct MAPK interaction. J Biol Chem 279:26959–26966

  33. Nakagami H, Pitzschke A, Hirt H (2005) Emerging MAP kinase pathways in plant stress signaling. Trend Plant Sci 10:339–346

  34. Nakashima K, Yamaguchi-Shinozaki K, Shinozaki K (2014) The transcriptional regulatory network in the drought response and its crosstalk in abiotic stress responses including drought, cold, and heat. Front Plant Sci 5:170

  35. Rabara RC, Tripathi P, Rushton PJ (2014) The potential of transcription factor-based genetic engineering in improving crop tolerance to drought. OMICS 18:601–614

  36. Rodriguez MC, Petersen M, Mundy J (2009) GhMPK7, a novel multiple stress-responsive cotton group C MAPK gene, has a role in broad spectrum disease resistance and plant development. Plant Mol Biol 74:1–17

  37. Saijo Y, Hata S, Kyozuka J et al (2010) Over-expression of a single Ca2+-dependent protein kinase confers both cold and salt/drought tolerance on rice plants. Plant J 23:319–327

  38. Seki M, Umezawa T, Urano K et al (2007) Regulatory metabolic networks in drought stress responses. Curr Opin Plant Biol 10:296–302

  39. Shi G, Fu J, Rong L, Zhang P, Guo C, Xiao K (2018) TaMIR1119, a miRNA family member of wheat (Triticum aestivum), is essential in the regulation of plant drought tolerance. J Integr Agric 17:2369–2378

  40. Tavakoli A, Ahmadi A, Alizadeh H (2009) A study of some physiological aspects of yield in drought tolerant vs susceptible wheat (Triticum aestivum L.) cultivars under post anthesis drought stress conditions. Iran J Field Crop Sci 15:134–142

  41. Tena G, Asai T, Chiu WL, Sheen J (2001) Plant mitogen-activated protein kinase signaling cascades. Curr Opin Plant Biol 4:392–400

  42. Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25:1105–1111

  43. Wang M, Zhang Y, Wang J, Wu X, Guo X (2007) MAP kinase gene in cotton (Gossypium hirsutum L.), GhMAPK, is involved in response to diverse environmental stresses. J Biochem Mol Biol 40:325–332

  44. Wang X, Vignjevic M, Jiang D, Jacobsen S, Wollenweber B (2014) Improved tolerance to drought stress after anthesis due to priming before anthesis in wheat (Triticum aestivum L.) var. Vinjett. J Exp Bot 65:6441–6456

  45. Wang L, Li Q, Lei Q, Feng C, Gao Y, Zheng X, Zhao Y, Wang Z, Kong J (2015a) MzPIP2;1: an aquaporin involved in radial water movement in both water uptake and transportation, altered the drought and salt tolerance of transgenic Arabidopsis. PLoS ONE 10:e0142446

  46. Wang A, Jia C, Li J, Xu B, Jin Z (2015b) Identification of six mitogen-activated protein kinase (MAPK) genes in banana (Musa acuminate L. AAA group, cv. Cavendish) under infection of Fusarium oxysporum f. sp. cubense Tropical Race 4. Acta Physiol Plant 37:115

  47. Wang Y, Zhang Y, Zhang R, Li J, Zhang M, Zhou S, Wang Z (2018) Reduced irrigation increases the water use efficiency and productivity of winter wheat-summer maize rotation on the North China Plain. Sci Total Environ 618:112–120

  48. White CA, Sylvester-Bradley R, Berry PM (2015) Root length densities of UK wheat and oilseed rape crops with implications for water capture and yield. J Exp Bot 66:2293–2303

  49. Xie C, Mao X, Huang J, Ding Y, Wu J, Dong S, Kong L, Gao G, Li C, Wei L (2011) KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acid Res 39:316–322

  50. Yang RC, Jana S, Clarke JM (1991) Phenotypic diversity and associations of some potentially drought-responsive characters in durum wheat. Crop Sci 31:1484–1491

  51. Yang M, Zhao Y, Shi S et al (2017) Wheat nuclear factor Y (NF-Y) B subfamily gene TaNF-YB3;l confers critical drought tolerance through modulation of the ABA-associated signaling pathway. Plant Cell Tiss Organ Cult 128:97–111

  52. Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acid Res 34:293–297

  53. Zhang J, Wang G, Zhou D, Xiao K (2018) Yield formation capacity, soil water consumption, property, and plant water use efficiency of wheat under water-saving conditions in North China plain. Turk J Field Crop 23:107–116

  54. Zou JJ, Wei FJ, Wang C, Wu JJ, Ratnasekera D, Liu WX, Wu WH (2010) Arabidopsis calcium-dependent protein kinase CPK10 functions in abscisic acid- and Ca2+-mediated stomatal regulation in response to drought stress. Plant Physiol 154:1232–1243

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Acknowledgements

This work was financially supported by Chinese National Key Research and Development Project on Science and Technology (2017YFD0300902) and the National Natural Science Foundation of China (No. 31872869 and No. 31671686).

Author information

KX designed the research. YZ, PD, XB, and RL conducted the experiment and performed data analysis. KX wrote the paper.

Correspondence to Kai Xiao.

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Zhao, Y., Du, P., Chen, Z. et al. Characterization on the water deprivation-associated physiological traits as well as the related differential genes during seed filling stage in wheat (T. aestivum L.). Plant Cell Tiss Organ Cult 140, 605–618 (2020). https://doi.org/10.1007/s11240-019-01756-7

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Keywords

  • Wheat (Triticum astivum L.)
  • Deficit irrigation
  • Osmolytes
  • Transcriptome analysis
  • Differentially expressed gene
  • Transgene analysis