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ANAC019 is required for recovery of reproductive development under drought stress in Arabidopsis

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Morphological and transcriptomic evidences provide us strong support for the function of ANAC019 in reproductive development under drought stress.

Abstract

Plants are sensitive to drought conditions, particularly at the reproductive stage. Several studies have reported drought effects on crop reproductive development, but the molecular mechanism underlying drought response during reproduction is still unclear. A recent study showed that drought induces in Arabidopsis inflorescence increased expression of many genes, including ANAC019. However, the function of ANAC019 in drought response during reproductive development has not been characterized. Here, we report an investigation of the ANAC019 function in the response to drought during reproduction. ANAC019 is preferentially expressed in the inflorescence compared with the leaf, suggesting possible roles in regulating both stress response and flower development. The anac019 mutant was more sensitive to drought than WT plant, and exhibited a delay in recovery of floral organ development under prolonged drought stress. Moreover, many fewer genes were differentially expressed in the anac019 inflorescence under drought than that of WT, suggesting that the mutant was impaired in drought-induced gene expression. The genes affected by ANAC019 were associated with stress and hormone responses as well as floral development. In particular, the expression levels of several key drought-induced genes, DREB2A, DREB2B, ARF2, MYB21 and MYB24, were dramatically reduced in the absence of ANAC019, suggesting that ANAC019 is an upstream regulator these genes for drought response and flower development. These results provide strong support for the potential function of ANAC019 in reproductive development under drought stress.

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References

  • Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63–78

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aida M, Ishida T, Fukaki H, Fujisawa H, Tasaka M (1997) Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. Plant Cell 9:841–857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alexander MP (1969) Differential staining of aborted and nonaborted pollen. Stain Technol 44:117–122

    Article  CAS  PubMed  Google Scholar 

  • Boonjung H, Fukai S (1996) Effects of soil water deficit at different growth stages on rice growth and yield under upland conditions. Field Crops Res 48:47–55

    Article  Google Scholar 

  • Bu Q, Jiang H, Li CB, Zhai Q, Zhang J, Wu X, Sun J, Xie Q, Li C (2008) Role of the Arabidopsis thaliana NAC transcription factors ANAC019 and ANAC055 in regulating jasmonic acid-signaled defense responses. Cell Res 18:756–767

    Article  PubMed  Google Scholar 

  • Chen H, Lai Z, Shi J, Xiao Y, Chen Z, Xu X (2010) Roles of Arabidopsis WRKY18, WRKY40 and WRKY60 transcription factors in plant responses to abscisic acid and abiotic stress. BMC Plant Biol 10:281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng H, Song S, Xiao L, Soo HM, Cheng Z, Xie D, Peng J (2009) Gibberellin acts through jasmonate to control the expression of MYB21, MYB24, and MYB57 to promote stamen filament growth in Arabidopsis. PLoS Genet 5:e1000440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chevalier D, Batoux M, Fulton L, Pfister K, Yadav RK, Schellenberg M, Schneitz K (2005) STRUBBELIG defines a receptor kinase-mediated signaling pathway regulating organ development in Arabidopsis. Proc Natl Acad Sci USA 102:9074–9079

    Article  CAS  PubMed  Google Scholar 

  • Chinnusamy V, Zhu J, Zhu JK (2006) Salt stress signaling and mechanisms of plant salt tolerance. Genet Eng (N Y) 27:141–177

    Article  CAS  Google Scholar 

  • Creelman RA, Mullet JE (1995) Jasmonic acid distribution and action in plants: regulation during development and response to biotic and abiotic stress. Proc Natl Acad Sci USA 92:4114–4119

    Article  CAS  PubMed  Google Scholar 

  • de Nadal E, Ammerer G, Posas F (2011) Controlling gene expression in response to stress. Nat Rev Genet 12:833–845

    Article  CAS  PubMed  Google Scholar 

  • Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38:W64–W70

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ellis CM, Nagpal P, Young JC, Hagen G, Guilfoyle TJ, Reed JW (2005) AUXIN RESPONSE FACTOR1 and AUXIN RESPONSE FACTOR2 regulate senescence and floral organ abscission in Arabidopsis thaliana. Development 132:4563–4574

    Article  CAS  PubMed  Google Scholar 

  • Fujita M, Fujita Y, Maruyama K, Seki M, Hiratsu K, Ohme-Takagi M, Tran LS, Yamaguchi-Shinozaki K, Shinozaki K (2004) A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant J 39:863–876

    Article  CAS  PubMed  Google Scholar 

  • He XJ, Mu RL, Cao WH, Zhang ZG, Zhang JS, Chen SY (2005) AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. Plant J 44:903–916

    Article  CAS  PubMed  Google Scholar 

  • Herrero MP, Johnson RR (1981) Drought stress and its effects on maize reproductive systems. Crop Sci 21:105–110

    Article  Google Scholar 

  • Hickman R, Hill C, Penfold CA, Breeze E, Bowden L, Moore JD, Zhang P, Jackson A, Cooke E, Bewicke-Copley F, Mead A, Beynon J, Wild DL, Denby KJ, Ott S, Buchanan-Wollaston V (2013) A local regulatory network around three NAC transcription factors in stress responses and senescence in Arabidopsis leaves. Plant J 75:26–39

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu W, Wang Y, Bowers C, Ma H (2003) Isolation, sequence analysis, and expression studies of florally expressed cDNAs in Arabidopsis. Plant Mol Biol 53:545–563

    Article  CAS  PubMed  Google Scholar 

  • Hu Y, Dong Q, Yu D (2012) Arabidopsis WRKY46 coordinates with WRKY70 and WRKY53 in basal resistance against pathogen Pseudomonas syringae. Plant Sci 185–186:288–297

    Article  CAS  PubMed  Google Scholar 

  • Jensen MK, Kjaersgaard T, Nielsen MM, Galberg P, Petersen K, O’Shea C, Skriver K (2010) The Arabidopsis thaliana NAC transcription factor family: structure-function relationships and determinants of ANAC019 stress signalling. Biochem J 426:183–196

    Article  PubMed  Google Scholar 

  • Jiang Y, Deyholos MK (2009) Functional characterization of Arabidopsis NaCl-inducible WRKY25 and WRKY33 transcription factors in abiotic stresses. Plant Mol Biol 69:91–105

    Article  CAS  PubMed  Google Scholar 

  • Jiang H, Li H, Bu Q, Li C (2009) The RHA2a-interacting proteins ANAC019 and ANAC055 may play a dual role in regulating ABA response and jasmonate response. Plant Signal Behav 4:464–466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kazan K, Manners JM (2013) MYC2: the master in action. Mol Plant 6:686–703

    Article  CAS  PubMed  Google Scholar 

  • Krishnaswamy S, Verma S, Rahman MH, Kav NN (2011) Functional characterization of four APETALA2-family genes (RAP2. RAP2.6L, DREB19 and DREB26) in Arabidopsis. Plant Mol Biol 75:107–127

    Article  CAS  PubMed  Google Scholar 

  • Krogan NT, Hogan K, Long JA (2012) APETALA2 negatively regulates multiple floral organ identity genes in Arabidopsis by recruiting the co-repressor TOPLESS and the histone deacetylase HDA19. Development 139:4180–4190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lalonde S, Beebe DU, Saini HS (1997) Early signs of disruption of wheat anther development associated with the induction of male sterility by meiotic-stage water deficit. Sex Plant Reprod 10:40–48

    Article  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(–Delta Delta C(T)) Method. Methods 25:402–408

    Article  CAS  Google Scholar 

  • Ma X, Sukiran NL, Ma H, Su Z (2014) Moderate drought causes dramatic floral transcriptomic reprogramming to ensure successful reproductive development in Arabidopsis. BMC Plant Biol 14:164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mandaokar A, Thines B, Shin B, Lange BM, Choi G, Koo YJ, Yoo YJ, Choi YD, Browse J (2006) Transcriptional regulators of stamen development in Arabidopsis identified by transcriptional profiling. Plant J 46:984–1008

    Article  CAS  PubMed  Google Scholar 

  • Mitsuda N, Seki M, Shinozaki K, Ohme-Takagi M (2005) The NAC transcription factors NST1 and NST2 of Arabidopsis regulate secondary wall thickenings and are required for anther dehiscence. Plant Cell 17:2993–3006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moss GI, Downey LA (1971) Influence of drought stress on female gametophyte development in corn (Zea mays L.) and subsequent grain yield. Crop Sci 11:368–372

    Article  Google Scholar 

  • Nagpal P, Ellis CM, Weber H, Ploense SE, Barkawi LS, Guilfoyle TJ, Hagen G, Alonso JM, Cohen JD, Farmer EE, Ecker JR, Reed JW (2005) Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development 132:4107–4118

    Article  CAS  PubMed  Google Scholar 

  • Nakashima K, Shinwari ZK, Sakuma Y, Seki M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2000) Organization and expression of two Arabidopsis DREB2 genes encoding DRE-binding proteins involved in dehydration- and high-salinity-responsive gene expression. Plant Mol Biol 42:657–665

    Article  CAS  PubMed  Google Scholar 

  • Nuruzzaman M, Sharoni AM, Kikuchi S (2013) Roles of NAC transcription factors in the regulation of biotic and abiotic stress responses in plants. Front Microbiol 4:248

    Article  PubMed  PubMed Central  Google Scholar 

  • Ogawa M, Kay P, Wilson S, Swain SM (2009) ARABIDOPSIS DEHISCENCE ZONE POLYGALACTURONASE1 (ADPG1), ADPG2, and QUARTET2 are polygalacturonases required for cell separation during reproductive development in Arabidopsis. Plant Cell 21:216–233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okushima Y, Mitina I, Quach HL, Theologis A (2005) AUXIN RESPONSE FACTOR 2 (ARF2): a pleiotropic developmental regulator. Plant J 43:29–46

    Article  CAS  PubMed  Google Scholar 

  • Oliver SN, Van Dongen JT, Alfred SC, Mamun EA, Zhao XC, Saini HS, Fernandes SF, Blanchard CL, Sutton BG, Geigenberger P, Dennis ES, Dolferus R (2005) Cold-induced repression of the rice anther-specific cell wall invertase gene OsINV4 is correlated with sucrose accumulation and pollen sterility. Plant Cell Environ 28:1534–1551

    Article  CAS  Google Scholar 

  • Puranik S, Sahu PP, Srivastava PS, Prasad M (2012) NAC proteins: regulation and role in stress tolerance. Trends Plant Sci 17:369–381

    Article  CAS  PubMed  Google Scholar 

  • Reeves PH, Ellis CM, Ploense SE, Wu MF, Yadav V, Tholl D, Chetelat A, Haupt I, Kennerley BJ, Hodgens C, Farmer EE, Nagpal P, Reed JW (2012) A regulatory network for coordinated flower maturation. PLoS Genet 8:e1002506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riboni M, Galbiati M, Tonelli C, Conti L (2013) GIGANTEA enables drought escape response via abscisic acid-dependent activation of the florigens and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS. Plant Physiol 162:1706–1719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rubio-Somoza I, Weigel D (2013) Coordination of flower maturation by a regulatory circuit of three microRNAs. PLoS Genet 9:e1003374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rushton DL, Tripathi P, Rabara RC, Lin J, Ringler P, Boken AK, Langum TJ, Smidt L, Boomsma DD, Emme NJ, Chen X, Finer JJ, Shen QJ, Rushton PJ (2012) WRKY transcription factors: key components in abscisic acid signalling. Plant Biotechnol J 10:2–11

    Article  CAS  PubMed  Google Scholar 

  • Sablowski RW, Meyerowitz EM (1998) A homolog of NO APICAL MERISTEM is an immediate target of the floral homeotic genes APETALA3/PISTILLATA. Cell 92:93–103

    Article  CAS  PubMed  Google Scholar 

  • Saini HS (1997) Effects of water stress on male gametophyte development in plants. Sex Plant Reprod 10:67–73

    Article  Google Scholar 

  • Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Biophys Res Commun 290:998–1009

    Article  CAS  PubMed  Google Scholar 

  • Sakuma Y, Maruyama K, Osakabe Y, Qin F, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18:1292–1309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scholl RL, May ST, Ware DH (2000) Seed and molecular resources for Arabidopsis. Plant Physiol 124:1477–1480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schruff MC, Spielman M, Tiwari S, Adams S, Fenby N, Scott RJ (2006) The AUXIN RESPONSE FACTOR 2 gene of Arabidopsis links auxin signalling, cell division, and the size of seeds and other organs. Development 133:251–261

    Article  CAS  PubMed  Google Scholar 

  • Schweizer F, Bodenhausen N, Lassueur S, Masclaux FG, Reymond P (2013) Differential contribution of transcription factors to Arabidopsis thaliana defense against Spodoptera littoralis. Front Plant Sci 4:13

    Article  PubMed  PubMed Central  Google Scholar 

  • Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T, Satou M, Akiyama K, Taji T, Yamaguchi-Shinozaki K, Carninci P, Kawai J, Hayashizaki Y, Shinozaki K (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31:279–292

    Article  CAS  PubMed  Google Scholar 

  • Seo PJ, Kim MJ, Park JY, Kim SY, Jeon J, Lee YH, Kim J, Park CM (2010) Cold activation of a plasma membrane-tethered NAC transcription factor induces a pathogen resistance response in Arabidopsis. Plant J 61:661–671

    Article  CAS  PubMed  Google Scholar 

  • Sheoran IS, Saini HS (1996) Drought-induced male sterility in rice: changes in carbohydrate levels and enzyme activities associated with the inhibition of starch accumulation in pollen. Sex Plant Reprod 9:161–169

    Article  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (1996) Molecular responses to drought and cold stress. Curr Opin Biotechnol 7:161–167

    Article  CAS  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (1997) Gene expression and signal transduction in water-stress response. Plant Physiol 115:327–334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227

    Article  CAS  PubMed  Google Scholar 

  • Smart RE (1974) Rapid estimates of relative water content. Plant Physiol 53:258–260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Su Z, Ma X, Guo H, Sukiran NL, Guo B, Assmann SM, Ma H (2013) Flower development under drought stress: morphological and transcriptomic analyses reveal acute responses and long-term acclimation in Arabidopsis. Plant Cell 25:3785–3807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Szecsi J, Joly C, Bordji K, Varaud E, Cock JM, Dumas C, Bendahmane M (2006) BIGPETALp, a bHLH transcription factor is involved in the control of Arabidopsis petal size. EMBO J 25:3912–3920

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tabata R, Ikezaki M, Fujibe T, Aida M, Tian CE, Ueno Y, Yamamoto KT, Machida Y, Nakamura K, Ishiguro S (2010) Arabidopsis AUXIN RESPONSE FACTOR6 and 8 regulate jasmonic acid biosynthesis and floral organ development via repression of class 1 KNOX genes. Plant Cell Physiol 51:164–175

    Article  CAS  PubMed  Google Scholar 

  • 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 37:914–939

    Article  CAS  PubMed  Google Scholar 

  • Tran LS, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama K, Fujita M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell 16:2481–2498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Winkel T, Renno J-F, Payne WA (1997) Effect of the timing of water deficit on growth, phenology and yield of pearl millet (Pennisetum glaucum (L.) R. Br.) grown in Sahelian conditions. J Exp Bot 48:1001–1009

    Article  CAS  Google Scholar 

  • Woodward C, Bemis SM, Hill EJ, Sawa S, Koshiba T, Torii KU (2005) Interaction of auxin and ERECTA in elaborating Arabidopsis inflorescence architecture revealed by the activation tagging of a new member of the YUCCA family putative flavin monooxygenases. Plant Physiol 139:192–203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wopereis MCS, Kropff MJ, Maligaya AR, Tuong TP (1996) Drought-stress responses of two lowland rice cultivars to soil water status. Field Crops Res 46:21–39

    Article  Google Scholar 

  • Xie Q, Frugis G, Colgan D, Chua NH (2000) Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev 14:3024–3036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiong L, Zhu JK (2002) Molecular and genetic aspects of plant responses to osmotic stress. Plant Cell Environ 25:131–139

    Article  CAS  PubMed  Google Scholar 

  • Yadav RK, Fulton L, Batoux M, Schneitz K (2008) The Arabidopsis receptor-like kinase STRUBBELIG mediates inter-cell-layer signaling during floral development. Dev Biol 323:261–270

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi M, Ohtani M, Mitsuda N, Kubo M, Ohme-Takagi M, Fukuda H, Demura T (2010) VND-INTERACTING2, a NAC domain transcription factor, negatively regulates xylem vessel formation in Arabidopsis. Plant Cell 22:1249–1263

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi-Shinozaki K, Koizumi M, Urao S, Shinozaki K (1992) Molecular cloning and characterization of 9 cDNAs for genes that are responsive to desiccation in Arabidopsis thaliana: Sequence analysis of one cDNA clone that encodes a putative transmembrane channel protein. Plant Cell Physiol 33:217–224

    Article  CAS  Google Scholar 

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Acknowledgements

We greatly appreciate the help of Dr Craig Praul of Genomics Core Facility for performing microarray hybridizations. We also express appreciation to Ms. Yi Hu for help with plant care.

Funding

This work was supported by a grant from the US Department of Energy (Grant No. DE-FG02-02ER15332) to H.M. and funds from Rijk Zwaan, the Biology Department and the Huck Institutes of the Life Sciences at the Pennsylvania State University.

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Authors and Affiliations

  1. Department of Biology and the Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA, 16802, USA

    Noor Liyana Sukiran, Hong Ma & Zhao Su

  2. State College Area High School, State College, PA, 16801, USA

    Julia C. Ma

  3. Center of Biotechnology and Functional Food, Faculty of Science and Technology, Universiti Kebangsaan Malaysia, 43600 UKM, Bangi, Selangor, Malaysia

    Noor Liyana Sukiran

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  1. Noor Liyana Sukiran
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ZS and HM designed the research. NLS and JCM performed different aspects of the research. NLS, ZS and HM wrote the article.

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Correspondence to Hong Ma or Zhao Su.

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Sukiran, N.L., Ma, J.C., Ma, H. et al. ANAC019 is required for recovery of reproductive development under drought stress in Arabidopsis. Plant Mol Biol 99, 161–174 (2019). https://doi.org/10.1007/s11103-018-0810-1

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