Integrating Transcriptome and Chromatin Landscapes for Deciphering the Epigenetic Regulation of Drought Response in Maize

  • Cristian Forestan
  • Silvia Farinati
  • Alice Lunardon
  • Serena Varotto
Part of the Compendium of Plant Genomes book series (CPG)


Water scarcity associated with climate change is among the principal constraints to plant productivity worldwide, and crop growth models predict that this issue will be more severe in future. Plants withstand drought stress by modifying their gene expression patterns and activating a variety of physiological and biochemical responses at cellular and whole-organism levels. Molecular and genomic studies have indeed identified many stress-inducible genes in different plant species. Stress-responsive genes encode for proteins with various functions and signaling factors, such as transcription factors, protein kinases, and protein phosphatases, but also include several noncoding and regulatory RNAs involved in the modulation of the stress response networks, making it a very complex phenomenon. Affecting a number of different aspects of plant growth and development, chromatin-based mechanisms, such as histone post-translational modifications, are fundamental for the fine coordination and tuning of gene expression in response to environmental cues. Several histone modifications have been found dramatically altered on stress-responsive gene regions under drought stress; thus, the integration of different omics technologies are essential to deeply understand plant tolerance mechanisms and manage them toward breeding for drought tolerance in maize.



Thanks to Vincenzo Rossi and Giulio Pavesi for their precious support on ChIP-Seq. This work was conducted within the grants from the European Commission (FP7 Project KBBE 2009 226477—“AENEAS”: Acquired Environmental Epigenetics Advances: from Arabidopsis to maize) and Italian MIUR-CNR Flagship project EPIGEN.


  1. Abdul Jaleel C, Manivannan P, Wahid A, Farooq M, Jasim Al-Juburi H, Somasundaram R, Panneerselvam R (2009) Drought stress in plants: a review on morphological characteristics and pigments compositionGoogle Scholar
  2. Agarwal PK, Gupta K, Lopato S, Agarwal P (2017) Dehydration responsive element binding transcription factors and their applications for the engineering of stress tolerance. J Exp Bot 68:2135–2148PubMedCrossRefPubMedCentralGoogle Scholar
  3. Asensi-Fabado MA, Amtmann A, Perrella G (2017) Plant responses to abiotic stress: the chromatin context of transcriptional regulation. Biochim Biophys Acta 1860:106–122CrossRefGoogle Scholar
  4. Augustine SM, Ashwin Narayan J, Syamaladevi DP, Appunu C, Chakravarthi M, Ravichandran V, Tuteja N, Subramonian N (2015) Overexpression of EaDREB2 and pyramiding of EaDREB2 with the pea DNA helicase gene (PDH45) enhance drought and salinity tolerance in sugarcane (Saccharum spp. hybrid). Plant Cell Rep 34:247–263PubMedCrossRefPubMedCentralGoogle Scholar
  5. Avramova Z (2015) Transcriptional ‘memory’ of a stress: transient chromatin and memory (epigenetic) marks at stress-response genes. Plant J 83:149–159PubMedCrossRefPubMedCentralGoogle Scholar
  6. Axtell MJ (2013) Classification and comparison of small RNAs from plants. Annu Rev Plant Biol 64:137–159PubMedCrossRefPubMedCentralGoogle Scholar
  7. Banziger M, Araus J (2007) Recent advances in breeding maize for drought and salinity stress tolerance. In: Jenks MA, Hasegawa PM, Jain SM (eds) Advances in molecular breeding toward drought and salt tolerant crops. Springer, Netherlands, Dordrecht, pp 587–601CrossRefGoogle Scholar
  8. Baucom RS, Estill JC, Chaparro C, Upshaw N, Jogi A, Deragon JM, Westerman RP, Sanmiguel PJ, Bennetzen JL (2009) Exceptional diversity, non-random distribution, and rapid evolution of retroelements in the B73 maize genome. PLoS Genet 5:e1000732PubMedPubMedCentralCrossRefGoogle Scholar
  9. Blum A (2014) Genomics for drought resistance—getting down to earthCrossRefGoogle Scholar
  10. Brands A, Ho TH (2002) Function of a plant stress-induced gene, HVA22. Synthetic enhancement screen with its yeast homolog reveals its role in vesicular traffic. Plant Physiol 130:1121–1131PubMedPubMedCentralCrossRefGoogle Scholar
  11. Cai R, Dai W, Zhang C, Wang Y, Wu M, Zhao Y, Ma Q, Xiang Y, Cheng B (2017) The maize WRKY transcription factor ZmWRKY17 negatively regulates salt stress tolerance in transgenic Arabidopsis plants. Planta 246:1215–1231PubMedCrossRefPubMedCentralGoogle Scholar
  12. Chen WJ, Zhu T (2004) Networks of transcription factors with roles in environmental stress response. Trends Plant Sci 9:591–596PubMedCrossRefPubMedCentralGoogle Scholar
  13. Chen X (2012) Small RNAs in development—insights from plants. Curr Opin Genet Dev 22:361–367PubMedPubMedCentralCrossRefGoogle Scholar
  14. Chung PJ, Jung H, Jeong DH, Ha SH, Choi YD, Kim JK (2016) Transcriptome profiling of drought responsive noncoding RNAs and their target genes in rice. BMC Genomics 17:563-016-2997-3Google Scholar
  15. Conesa A, Madrigal P, Tarazona S, Gomez-Cabrero D, Cervera A, McPherson A, Szczesniak MW, Gaffney DJ, Elo LL, Zhang X, Mortazavi A (2016) A survey of best practices for RNA-seq data analysis. Genome Biol 17:13-016-0881-8Google Scholar
  16. Cook BI, Anchukaitis KJ, Touchan R, Meko DM, Cook ER (2016) Spatiotemporal drought variability in the Mediterranean over the last 900 years 121:2060–2074Google Scholar
  17. Cui M, Zhang W, Zhang Q, Xu Z, Zhu Z, Duan F, Wu R (2011) Induced over-expression of the transcription factor OsDREB2A improves drought tolerance in rice. Plant Physiol Biochem 49:1384–1391PubMedCrossRefGoogle Scholar
  18. Dai X, Wang Y, Zhang WH (2016) OsWRKY74, a WRKY transcription factor, modulates tolerance to phosphate starvation in rice. J Exp Bot 67:947–960PubMedPubMedCentralCrossRefGoogle Scholar
  19. Dey S, Corina Vlot A (2015) Ethylene responsive factors in the orchestration of stress responses in monocotyledonous plants. Front Plant Sci 6:640PubMedPubMedCentralCrossRefGoogle Scholar
  20. Di C, Yuan J, Wu Y, Li J, Lin H, Hu L, Zhang T, Qi Y, Gerstein MB, Guo Y, Lu ZJ (2014) Characterization of stress-responsive lncRNAs in Arabidopsis thaliana by integrating expression, epigenetic and structural features. Plant J 80:848–861PubMedCrossRefGoogle Scholar
  21. Ding ZJ, Yan JY, Xu XY, Yu DQ, Li GX, Zhang SQ, Zheng SJ (2014) Transcription factor WRKY46 regulates osmotic stress responses and stomatal movement independently in Arabidopsis. Plant J 79:13–27PubMedCrossRefPubMedCentralGoogle Scholar
  22. Du J, Johnson LM, Jacobsen SE, Patel DJ (2015) DNA methylation pathways and their crosstalk with histone methylation. Nat Rev Mol Cell Biol 16:519–532PubMedPubMedCentralCrossRefGoogle Scholar
  23. Erhard KF Jr, Talbot JE, Deans NC, McClish AE, Hollick JB (2015) Nascent transcription affected by RNA polymerase IV in Zea mays. Genetics 199:1107–1125PubMedPubMedCentralCrossRefGoogle Scholar
  24. Erhard KF, Stonaker JL, Parkinson SE, Lim JP, Hale CJ, Hollick JB (2009) RNA polymErase IV functions in paramutation in Zea mays. Science 323:1201–1205PubMedCrossRefPubMedCentralGoogle Scholar
  25. Forestan C, Aiese Cigliano R, Farinati S, Lunardon A, Sanseverino W, Varotto S (2016) Stress-induced and epigenetic-mediated maize transcriptome regulation study by means of transcriptome reannotation and differential expression analysis. Sci Rep 6:30446PubMedPubMedCentralCrossRefGoogle Scholar
  26. Guan C, Wu B, Yu T, Wang Q, Krogan NT, Liu X, Jiao Y (2017) Spatial auxin signaling controls leaf flattening in Arabidopsis. Curr Biol 27(2940–2950):e4Google Scholar
  27. Haak DC, Fukao T, Grene R, Hua Z, Ivanov R, Perrella G, Li S (2017) Multilevel regulation of abiotic stress responses in plants. Front Plant Sci 8:1564PubMedPubMedCentralCrossRefGoogle Scholar
  28. Harrison MT, Tardieu F, Dong Z, Messina CD, Hammer GL (2014) Characterizing drought stress and trait influence on maize yield under current and future conditions. Glob Chang Biol 20:867–878PubMedCrossRefPubMedCentralGoogle Scholar
  29. Hong Y, Zhang H, Huang L, Li D, Song F (2016) Overexpression of a stress-responsive NAC transcription factor gene ONAC022 improves drought and salt tolerance in rice. Front Plant Sci 7:4PubMedPubMedCentralCrossRefGoogle Scholar
  30. Iwaki T, Guo L, Ryals JA, Yasuda S, Shimazaki T, Kikuchi A, Watanabe KN, Kasuga M, Yamaguchi-Shinozaki K, Ogawa T, Ohta D (2013) Metabolic profiling of transgenic potato tubers expressing Arabidopsis dehydration response element-binding protein 1A (DREB1A). J Agric Food Chem 61:893–900PubMedCrossRefGoogle Scholar
  31. Jia J, Fu J, Zheng J, Zhou X, Huai J, Wang J, Wang M, Zhang Y, Chen X, Zhang J, Zhao J, Su Z, Lv Y, Wang G (2006) Annotation and expression profile analysis of 2073 full-length cDNAs from stress-induced maize (Zea mays L.) seedlings. Plant J 48:710–727PubMedCrossRefGoogle Scholar
  32. Joshi R, Wani SH, Singh B, Bohra A, Dar ZA, Lone AA, Pareek A, Singla-Pareek SL (2016) Transcription factors and plants response to drought stress: current understanding and future directions. Front Plant Sci 7:1029PubMedPubMedCentralCrossRefGoogle Scholar
  33. Kumar V, Khare T, Shriram V, Wani SH (2018) Plant small RNAs: the essential epigenetic regulators of gene expression for salt-stress responses and tolerance. Plant Cell Rep 37:61–75PubMedCrossRefGoogle Scholar
  34. Lamke J, Baurle I (2017) Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants. Genome Biol 18:124-017-1263-6Google Scholar
  35. Laraus J (2004) The problems of sustainable water use in the Mediterranean and research requirements for agriculture. Ann Appl Biol 144:259–272CrossRefGoogle Scholar
  36. Lembke CG, Nishiyama MY Jr, Sato PM, de Andrade RF, Souza GM (2012) Identification of sense and antisense transcripts regulated by drought in sugarcane. Plant Mol Biol 79:461–477PubMedPubMedCentralCrossRefGoogle Scholar
  37. Li H, Gao Y, Xu H, Dai Y, Deng D, Chen J (2013) ZmWRKY33, a WRKY maize transcription factor conferring enhanced salt stress tolerances in ArabidopsisGoogle Scholar
  38. Liu J, Wang H, Chua NH (2015) Long noncoding RNA transcriptome of plants. Plant Biotechnol J 13:319–328PubMedCrossRefGoogle Scholar
  39. Liu S, Wang X, Wang H, Xin H, Yang X, Yan J, Li J, Tran LS, Shinozaki K, Yamaguchi-Shinozaki K, Qin F (2013) Genome-wide analysis of ZmDREB genes and their association with natural variation in drought tolerance at seedling stage of Zea mays L. PLoS Genet 9:e1003790PubMedPubMedCentralCrossRefGoogle Scholar
  40. Lobell DB, Roberts MJ, Schlenker W, Braun N, Little BB, Rejesus RM, Hammer GL (2014) Greater sensitivity to drought accompanies maize yield increase in the U.S Midwest. Science 344:516–519PubMedCrossRefPubMedCentralGoogle Scholar
  41. Lu HF, Dong HT, Sun CB, Qing DJ, Li N, Wu ZK, Wang ZQ, Li YZ (2011) The panorama of physiological responses and gene expression of whole plant of maize inbred line YQ7-96 at the three-leaf stage under water deficit and re-watering. Theor Appl Genet 123:943–958PubMedCrossRefPubMedCentralGoogle Scholar
  42. Lunardon A, Forestan C, Farinati S, Axtell M, Varotto S (2016) Genome-wide characterization of maize small RNA loci and their regulation in the required to maintain repression6-1 (rmr6-1) mutant and long-term abiotic stresses. Plant Physiol 170:1535–1548PubMedPubMedCentralGoogle Scholar
  43. Makarevitch I, Waters AJ, West PT, Stitzer M, Hirsch CN, Ross-Ibarra J, Springer NM (2015) Transposable elements contribute to activation of maize genes in response to abiotic stress. PLoS Genet 11:e1004915PubMedPubMedCentralCrossRefGoogle Scholar
  44. Mao H, Wang H, Liu S, Li Z, Yang X, Yan J, Li J, Tran LS, Qin F (2015) A transposable element in a NAC gene is associated with drought tolerance in maize seedlings. Nat Commun 6:8326PubMedPubMedCentralCrossRefGoogle Scholar
  45. Matsui A, Nguyen AH, Nakaminami K, Seki M (2013) Arabidopsis non-coding RNA regulation in abiotic stress responses. Int J Mol Sci 14:22642–22654PubMedPubMedCentralCrossRefGoogle Scholar
  46. Matzke MA, Mosher RA (2014) RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat Rev Genet 15:394–408PubMedCrossRefPubMedCentralGoogle Scholar
  47. Mecchia MA, Debernardi JM, Rodriguez RE, Schommer C, Palatnik JF (2013) MicroRNA miR396 and RDR6 synergistically regulate leaf development. Mech Dev 130:2–13PubMedCrossRefPubMedCentralGoogle Scholar
  48. Miao Z, Han Z, Zhang T, Chen S, Ma C (2017) A systems approach to a spatio-temporal understanding of the drought stress response in maize. Sci Rep 7:6590-017-06929-yGoogle Scholar
  49. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410CrossRefGoogle Scholar
  50. Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) AP2/ERF family transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819:86–96PubMedPubMedCentralCrossRefGoogle Scholar
  51. Moorhead GB, Trinkle-Mulcahy L, Ulke-Lemee A (2007) Emerging roles of nuclear protein phosphatases. Nat Rev Mol Cell Biol 8:234–244PubMedCrossRefPubMedCentralGoogle Scholar
  52. Morari F, Meggio F, Lunardon A, Scudiero E, Forestan C, Farinati S, Varotto S (2015) Time course of biochemical, physiological, and molecular responses to field-mimicked conditions of drought, salinity, and recovery in two maize lines. Front Plant Sci 6:314PubMedPubMedCentralCrossRefGoogle Scholar
  53. 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 5:170PubMedPubMedCentralCrossRefGoogle Scholar
  54. Okay S, Derelli E, Unver T (2014) Transcriptome-wide identification of bread wheat WRKY transcription factors in response to drought stress. Mol Genet Genomics 289:765–781PubMedCrossRefPubMedCentralGoogle Scholar
  55. Opitz N, Paschold A, Marcon C, Malik WA, Lanz C, Piepho HP, Hochholdinger F (2014) Transcriptomic complexity in young maize primary roots in response to low water potentials. BMC Genomics 15:741-2164-15-741PubMedPubMedCentralCrossRefGoogle Scholar
  56. Paul S, Gayen D, Datta SK, Datta K (2015) Dissecting root proteome of transgenic rice cultivars unravels metabolic alterations and accumulation of novel stress responsive proteins under drought stress. Plant Sci 234:133–143PubMedCrossRefGoogle Scholar
  57. Peragine A, Yoshikawa M, Wu G, Albrecht HL, Poethig RS (2004) SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. Genes Dev 18:2368–2379PubMedPubMedCentralCrossRefGoogle Scholar
  58. Phukan UJ, Jeena GS, Shukla RK (2016) WRKY transcription factors: molecular regulation and stress responses in plants. Front Plant Sci 7:760PubMedPubMedCentralCrossRefGoogle Scholar
  59. Qin T, Zhao H, Cui P, Albesher N, Xiong L (2017) A nucleus-localized long non-coding RNA enhances drought and salt stress tolerance. Plant Physiol 175:1321–1336PubMedPubMedCentralCrossRefGoogle Scholar
  60. Qiu Y, Yu D (2009) Over-expression of the stress-induced OsWRKY45 enhances disease resistance and drought tolerance in Arabidopsis. Environ Exp Bot 65:35–47CrossRefGoogle Scholar
  61. Riechmann JL, Meyerowitz EM (1998) The AP2/EREBP family of plant transcription factors. Biol Chem 379:633–646PubMedGoogle Scholar
  62. Rogers K, Chen X (2013) Biogenesis, turnover, and mode of action of plant microRNAs. Plant Cell 25:2383–2399PubMedPubMedCentralCrossRefGoogle Scholar
  63. Seager R, Tzanova A, Nakamura J (2009) Drought in the Southeastern United States: causes, variability over the last millennium, and the potential for future hydroclimate change. J Climate 22:5021–5045CrossRefGoogle Scholar
  64. Shan X, Li Y, Jiang Y, Jiang Z, Hao W, Yuan Y (2013) Transcriptome profile analysis of maize seedlings in response to high-salinity, drought and cold stresses by deep sequencing. Plant Mol Biol Rep 31:1485–1491CrossRefGoogle Scholar
  65. Shavrukov Y, Baho M, Lopato S, Langridge P (2016) The TaDREB3 transgene transferred by conventional crossings to different genetic backgrounds of bread wheat improves drought tolerance. Plant Biotechnol J 14:313–322PubMedCrossRefPubMedCentralGoogle Scholar
  66. Shen Q, Chen CN, Brands A, Pan SM, Ho TH (2001) The stress—and abscisic acid-induced barley gene HVA22: developmental regulation and homologues in diverse organisms. Plant Mol Biol 45:327–340PubMedCrossRefPubMedCentralGoogle Scholar
  67. Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227PubMedCrossRefPubMedCentralGoogle Scholar
  68. Singh B, Singh B, Kumar V, Pankaj Kumar S, Jayaswal PK, Shefali M, Singh N (2015) Haplotype diversity and association analysis of SNAC1 gene in wild rice germplasmGoogle Scholar
  69. Sunkar R, Kapoor A, Zhu JK (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18:2051–2065PubMedPubMedCentralCrossRefGoogle Scholar
  70. Thimm O, Blasing O, Gibon Y, Nagel A, Meyer S, Kruger P, Selbig J, Muller LA, Rhee SY, Stitt M (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37:914–939PubMedCrossRefPubMedCentralGoogle Scholar
  71. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7:562–578PubMedPubMedCentralCrossRefGoogle Scholar
  72. Trindade I, Capitao C, Dalmay T, Fevereiro MP, Santos DM (2010) miR398 and miR408 are up-regulated in response to water deficit in Medicago truncatula. Planta 231:705–716PubMedCrossRefPubMedCentralGoogle Scholar
  73. Usadel B, Poree F, Nagel A, Lohse M, Czedik-Eysenberg A, Stitt M (2009) A guide to using MapMan to visualize and compare Omics data in plants: a case study in the crop species, maize. Plant Cell Environ 32:1211–1229PubMedCrossRefGoogle Scholar
  74. Wang D, Qu Z, Yang L, Zhang Q, Liu ZH, Do T, Adelson DL, Wang ZY, Searle I, Zhu JK (2017a) Transposable elements (TEs) contribute to stress-related long intergenic noncoding RNAs in plants. Plant J 90:133–146PubMedPubMedCentralCrossRefGoogle Scholar
  75. Wang H, Wang H, Shao H, Tang X (2016) Recent advances in utilizing transcription factors to improve plant abiotic stress tolerance by transgenic technology. Front Plant Sci 7:67PubMedPubMedCentralGoogle Scholar
  76. Wang J, Meng X, Dobrovolskaya OB, Orlov YL, Chen M (2017b) Non-coding RNAs and their roles in stress response in plants. Genomics Proteomics Bioinform. 15:301–312CrossRefGoogle Scholar
  77. Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133:3539–3547PubMedPubMedCentralCrossRefGoogle Scholar
  78. Wu S, Ning F, Zhang Q, Wu X, Wang W (2017) Enhancing omics research of crop responses to drought under field conditions. Front Plant Sci 8:174PubMedPubMedCentralGoogle Scholar
  79. Wu X, Shiroto Y, Kishitani S, Ito Y, Toriyama K (2009) Enhanced heat and drought tolerance in transgenic rice seedlings overexpressing OsWRKY11 under the control of HSP101 promoter. Plant Cell Rep 28:21–30PubMedCrossRefGoogle Scholar
  80. Xu J, Wang Q, Freeling M, Zhang X, Xu Y, Mao Y, Tang X, Wu F, Lan H, Cao M, Rong T, Lisch D, Lu Y (2017) Natural antisense transcripts are significantly involved in regulation of drought stress in maize. Nucleic Acids Res 45:5126–5141PubMedPubMedCentralCrossRefGoogle Scholar
  81. Yamaguchi A, Wu MF, Yang L, Wu G, Poethig RS, Wagner D (2009) The microRNA-regulated SBP-Box transcription factor SPL3 is a direct upstream activator of LEAFY, FRUITFULL, and APETALA1. Dev Cell 17:268–278PubMedPubMedCentralCrossRefGoogle Scholar
  82. You J, Zong W, Hu H, Li X, Xiao J, Xiong L (2014) A STRESS-RESPONSIVE NAC1-regulated protein phosphatase gene rice protein phosphatase18 modulates drought and oxidative stress tolerance through abscisic acid-independent reactive oxygen species scavenging in rice. Plant Physiol 166:2100–2114PubMedPubMedCentralCrossRefGoogle Scholar
  83. Yu S, Ligang C, Liping Z, Diqiu Y (2010) Overexpression of OsWRKY72 gene interferes in the abscisic acid signal and auxin transport pathway of Arabidopsis. J Biosci 35:459–471PubMedCrossRefPubMedCentralGoogle Scholar
  84. Yuan L, Liu X, Luo M, Yang S, Wu K (2013) Involvement of histone modifications in plant abiotic stress responses. J Integr Plant Biol 55:892–901PubMedGoogle Scholar
  85. Zhang B, Pan X, Cannon CH, Cobb GP, Anderson TA (2006) Conservation and divergence of plant microRNA genes. Plant J 46:243–259PubMedCrossRefPubMedCentralGoogle Scholar
  86. Zhang W, Han Z, Guo Q, Liu Y, Zheng Y, Wu F, Jin W (2014) Identification of maize long non-coding RNAs responsive to drought stress. PLoS ONE 9:e98958PubMedPubMedCentralCrossRefGoogle Scholar
  87. Zhang YC, Chen YQ (2013) Long noncoding RNAs: new regulators in plant development. Biochem Biophys Res Commun 436:111–114PubMedCrossRefPubMedCentralGoogle Scholar
  88. Zhao L, Wang P, Yan S, Gao F, Li H, Hou H, Zhang Q, Tan J, Li L (2014) Promoter-associated histone acetylation is involved in the osmotic stress-induced transcriptional regulation of the maize ZmDREB2A gene. Physiol Plant 151:459–467PubMedCrossRefPubMedCentralGoogle Scholar
  89. Zhu C, Ding Y, Liu H (2011) MiR398 and plant stress responses. Physiol Plant 143:1–9PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Cristian Forestan
    • 1
  • Silvia Farinati
    • 1
  • Alice Lunardon
    • 2
  • Serena Varotto
    • 1
  1. 1.Department of Agronomy, Food, Natural resources, Animal and Environment (DAFNAE) AgripolisUniversity of PadovaLegnaroItaly
  2. 2.Department of Biology and Huck Institutes of the Life SciencesPenn State UniversityLos AngelesUSA

Personalised recommendations