A DAO1-Mediated Circuit Controls Auxin and Jasmonate Crosstalk Robustness during Adventitious Root Initiation in Arabidopsis

. 2019 Sep 09 ; 20 (18) : . [epub] 20190909

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid31505771

Adventitious rooting is a post-embryonic developmental program governed by a multitude of endogenous and environmental cues. Auxin, along with other phytohormones, integrates and translates these cues into precise molecular signatures to provide a coherent developmental output. Auxin signaling guides every step of adventitious root (AR) development from the early event of cell reprogramming and identity transitions until emergence. We have previously shown that auxin signaling controls the early events of AR initiation (ARI) by modulating the homeostasis of the negative regulator jasmonate (JA). Although considerable knowledge has been acquired about the role of auxin and JA in ARI, the genetic components acting downstream of JA signaling and the mechanistic basis controlling the interaction between these two hormones are not well understood. Here we provide evidence that COI1-dependent JA signaling controls the expression of DAO1 and its closely related paralog DAO2. In addition, we show that the dao1-1 loss of function mutant produces more ARs than the wild type, probably due to its deficiency in accumulating JA and its bioactive metabolite JA-Ile. Together, our data indicate that DAO1 controls a sensitive feedback circuit that stabilizes the auxin and JA crosstalk during ARI.

Zobrazit více v PubMed

Bellini C., Pacurar D.I., Perrone I. Adventitious Roots and Lateral Roots: Similarities and Differences. Annu. Rev. Plant Biol. 2014;65:639–666. doi: 10.1146/annurev-arplant-050213-035645. PubMed DOI

Steffens B., Rasmussen A. The Physiology of Adventitious Roots. Plant Physiol. 2016;170:603–617. doi: 10.1104/pp.15.01360. PubMed DOI PMC

Ikeuchi M., Favero D.S., Sakamoto Y., Iwase A., Coleman D., Rymen B., Sugimoto K. Molecular Mechanisms of Plant Regeneration. Annu. Rev. Plant Biol. 2019;70:377–406. doi: 10.1146/annurev-arplant-050718-100434. PubMed DOI

Lakehal A., Bellini C. Control of adventitious root formation: Insights into synergistic and antagonistic hormonal interactions. Physiol. Plant. 2018;165:90–100. doi: 10.1111/ppl.12823. PubMed DOI

Sukumar P., Maloney G.S., Muday G.K. Localized Induction of the ATP-Binding Cassette B19 Auxin Transporter Enhances Adventitious Root Formation in Arabidopsis. Plant Physiol. 2013;162:1392–1405. doi: 10.1104/pp.113.217174. PubMed DOI PMC

Chen L., Tong J., Xiao L., Ruan Y., Liu J., Zeng M., Huang H., Wang J.W., Xu L. YUCCA-mediated auxin biogenesis is required for cell fate transition occurring during de novo root organogenesis in Arabidopsis. J. Exp. Bot. 2016;67:4273–4284. doi: 10.1093/jxb/erw213. PubMed DOI PMC

Delarue M., Prinsen E., Van Onckelen H., Caboche M., Bellini C. Sur2 mutations of Arabidopsis thaliana define a new locus involved in the control of auxin homeostasis. Plant J. 1998;14:603–611. doi: 10.1046/j.1365-313X.1998.00163.x. PubMed DOI

Zhao Y. Essential Roles of Local Auxin Biosynthesis in Plant Development and in Adaptation to Environmental Changes. Annu. Rev. Plant Biol. 2018;69:417–435. doi: 10.1146/annurev-arplant-042817-040226. PubMed DOI

Ljung K. Auxin metabolism and homeostasis during plant development. Development. 2013;140:943–950. doi: 10.1242/dev.086363. PubMed DOI

Staswick P.E., Serban B., Rowe M., Tiryaki I., Marie M., Maldonado M.C., Suza W. Characterization of an Arabidopsis Enzyme Family That Conjugates Amino Acids to Indole-3-Acetic Acid. Plant Cell. 2005;17:616–627. doi: 10.1105/tpc.104.026690. PubMed DOI PMC

Zheng Z., Guo Y., Novák O., Chen W., Ljung K., Noel J.P., Chory J. Local auxin metabolism regulates environment induced hypocotyl elongation. Nat. Plants. 2016;2:1–9. doi: 10.1038/nplants.2016.25. PubMed DOI PMC

Park J.E., Park J.Y., Kim Y.S., Staswick P.E., Jeon J., Yun J., Kim S.Y., Kim J., Lee Y.H., Park C.M. GH3-mediated auxin homeostasis links growth regulation with stress adaptation response in Arabidopsis. J. Biol. Chem. 2007;282:10036–10046. doi: 10.1074/jbc.M610524200. PubMed DOI

Pencik A., Simonovik B., Petersson S.V., Henykova E., Simon S., Greenham K., Zhang Y., Kowalczyk M., Estelle M., Zazimalova E., et al. Regulation of Auxin Homeostasis and Gradients in Arabidopsis Roots through the Formation of the Indole-3-Acetic Acid Catabolite 2-Oxindole-3-Acetic Acid. Plant Cell. 2013;25:3858–3870. doi: 10.1105/tpc.113.114421. PubMed DOI PMC

Butler E.D., Gallagher T.F. Characterization of auxin-induced ARRO-1 expression in the primary root of Malus domestica. J. Exp. Bot. 2000;51:1765–1766. doi: 10.1093/jexbot/51.351.1765. PubMed DOI

Zhao Z., Zhang Y., Liu X., Zhang X., Liu S., Yu X., Ren Y., Zheng X., Zhou K., Jiang L., et al. A Role for a Dioxygenase in Auxin Metabolism and Reproductive Development in Rice. Dev. Cell. 2013;27:113–122. doi: 10.1016/j.devcel.2013.09.005. PubMed DOI

Zhang J., Lin J.E., Harris C., Campos Mastrotti Pereira F., Wu F., Blakeslee J.J., Peer W.A. DAO1 catalyzes temporal and tissue-specific oxidative inactivation of auxin in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA. 2016;113:11010–11015. doi: 10.1073/pnas.1604769113. PubMed DOI PMC

Porco S., Pěnčík A., Rashed A., Voß U., Casanova-Sáez R., Bishopp A., Golebiowska A., Bhosale R., Swarup R., Swarup K., et al. Dioxygenase-encoding AtDAO1 gene controls IAA oxidation and homeostasis in Arabidopsis. Proc. Natl. Acad. Sci. USA. 2016;113:11016–11021. doi: 10.1073/pnas.1604375113. PubMed DOI PMC

Mellor N., Band L.R., Pěnčík A., Novák O., Rashed A., Holman T., Wilson M.H., Voß U., Bishopp A., King J.R., et al. Dynamic regulation of auxin oxidase and conjugating enzymes AtDAO1 and GH3 modulates auxin homeostasis. Proc. Natl. Acad. Sci. USA. 2016;113:11022–11027. doi: 10.1073/pnas.1604458113. PubMed DOI PMC

Sun J., Xu Y., Ye S., Jiang H., Chen Q., Liu F., Zhou W., Chen R., Li X., Tietz O., et al. Arabidopsis ASA1 Is Important for Jasmonate-Mediated Regulation of Auxin Biosynthesis and Transport during Lateral Root Formation. Plant Cell. 2009;21:1495–1511. doi: 10.1105/tpc.108.064303. PubMed DOI PMC

Xie D.X., Feys B.F., James S., Nieto-Rostro M., Turner J.G. COI1: An Arabidopsis Gene Required for Jasmonate-Regulated Defense and Fertility. Science. 1998;280:1091–1094. doi: 10.1126/science.280.5366.1091. PubMed DOI

Sun J., Chen Q., Qi L., Jiang H., Li S., Xu Y., Liu F., Zhou W., Pan J., Li X., et al. Jasmonate modulates endocytosis and plasma membrane accumulation of the arabidopsis pin2 protein. New Phytol. 2011;191:360–375. doi: 10.1111/j.1469-8137.2011.03713.x. PubMed DOI

Gutierrez L., Mongelard G., Floková K., Păcurar D.I., Novák O., Staswick P., Kowalczyk M., Păcurar M., Demailly H., Geiss G., et al. Auxin Controls Arabidopsis Adventitious Root Initiation by Regulating Jasmonic Acid Homeostasis. Plant Cell. 2012;24:2515–2527. doi: 10.1105/tpc.112.099119. PubMed DOI PMC

Nagpal P., Ellis C.M., Weber H., Ploense S.E., Barkawi L.S., Guilfoyle T.J., Hagen G., Alonso J.M., Cohen J.D., Farmer E.E., et al. Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development. 2005;132:4107–4118. doi: 10.1242/dev.01955. PubMed DOI

Cecchetti V., Altamura M.M., Brunetti P., Petrocelli V., Falasca G., Ljung K., Costantino P., Cardarelli M. Auxin controls arabidopsis anther dehiscence by regulating endothecium lignification and jasmonic acid biosynthesis. Plant J. 2013;74:411–422. doi: 10.1111/tpj.12130. PubMed DOI

An C., Li L., Zhai Q., You Y., Deng L., Wu F., Chen R., Jiang H., Wang H., Chen Q., et al. Mediator subunit MED25 links the jasmonate receptor to transcriptionally active chromatin. Proc. Natl. Acad. Sci. USA. 2017;114:E8930–E8939. doi: 10.1073/pnas.1710885114. PubMed DOI PMC

Pauwels L., Morreel K., De Witte E., Lammertyn F., Van Montagu M., Boerjan W., Inze D., Goossens A. Mapping methyl jasmonate-mediated transcriptional reprogramming of metabolism and cell cycle progression in cultured Arabidopsis cells. Proc. Natl. Acad. Sci. USA. 2008;105:1380–1385. doi: 10.1073/pnas.0711203105. PubMed DOI PMC

Hickman R., Van Verk M.C., Van Dijken A.J.H., Mendes M.P., Vroegop-Vos I.A., Caarls L., Steenbergen M., Van der Nagel I., Wesselink G.J., Jironkin A., et al. Architecture and Dynamics of the Jasmonic Acid Gene Regulatory Network. Plant Cell. 2017;29:2086–2105. doi: 10.1105/tpc.16.00958. PubMed DOI PMC

Winter D., Vinegar B., Nahal H., Ammar R., Wilson G.V., Provart N.J. An “electronic fluorescent pictograph” Browser for exploring and analyzing large-scale biological data sets. PLoS ONE. 2007;2:e718. doi: 10.1371/journal.pone.0000718. PubMed DOI PMC

Zhang G., Zhao F., Chen L., Pan Y., Sun L., Bao N., Zhang T., Cui C.X., Qiu Z., Zhang Y., et al. Jasmonate-mediated wound signalling promotes plant regeneration. Nat. Plants. 2019;5:491–497. doi: 10.1038/s41477-019-0408-x. PubMed DOI

Godoy M., Franco-Zorrilla J.M., Pérez-Pérez J., Oliveros J.C., Lorenzo Ó., Solano R. Improved protein-binding microarrays for the identification of DNA-binding specificities of transcription factors. Plant J. 2011;66:700–711. doi: 10.1111/j.1365-313X.2011.04519.x. PubMed DOI

Cai X.T., Xu P., Zhao P.X., Liu R., Yu L.H., Xiang C. Bin Arabidopsis ERF109 mediates cross-talk between jasmonic acid and auxin biosynthesis during lateral root formation. Nat. Commun. 2014;5:1–13. doi: 10.1038/ncomms6833. PubMed DOI

Hentrich M., Böttcher C., Düchting P., Cheng Y., Zhao Y., Berkowitz O., Masle J., Medina J., Pollmann S. The jasmonic acid signaling pathway is linked to auxin homeostasis through the modulation of YUCCA8 and YUCCA9 gene expression. Plant J. 2013;74:626–637. doi: 10.1111/tpj.12152. PubMed DOI PMC

Hayashi K.I., Neve J., Hirose M., Kuboki A., Shimada Y., Kepinski S., Nozaki H. Rational design of an auxin antagonist of the SCF TIR1 auxin receptor complex. ACS Chem. Biol. 2012;7:590–598. doi: 10.1021/cb200404c. PubMed DOI

Gutierrez L., Bussell J.D., Pacurar D.I., Schwambach J., Pacurar M., Bellini C. Phenotypic Plasticity of Adventitious Rooting in Arabidopsis Is Controlled by Complex Regulation of AUXIN RESPONSE FACTOR Transcripts and MicroRNA Abundance. Plant Cell. 2009;21:3119–3132. doi: 10.1105/tpc.108.064758. PubMed DOI PMC

Sorin C., Bussell J.D., Camus I., Ljung K., Kowalczyk M., Geiss G., McKhann H., Garcion C., Vaucheret H., Sandberg G., et al. Auxin and Light Control of Adventitious Rooting in Arabidopsis. Plant Cell. 2005;17:1343–1359. doi: 10.1105/tpc.105.031625. PubMed DOI PMC

Chen L.R., Chen Y.J., Lee C.Y., Lin T.Y. MeJA-induced transcriptional changes in adventitious roots of Bupleurum kaoi. Plant Sci. 2007;173:12–24. doi: 10.1016/j.plantsci.2007.03.013. DOI

Lischweski S., Muchow A., Guthörl D., Hause B. Jasmonates act positively in adventitious root formation in petunia cuttings. BMC Plant Biol. 2015;15:229. doi: 10.1186/s12870-015-0615-1. PubMed DOI PMC

Fernández-Calvo P., Chini A., Fernández-Barbero G., Chico J.M., Gimenez-Ibanez S., Geerinck J., Eeckhout D., Schweizer F., Godoy M., Franco-Zorrilla J.M., et al. The Arabidopsis bHLH Transcription Factors MYC3 and MYC4 Are Targets of JAZ Repressors and Act Additively with MYC2 in the Activation of Jasmonate Responses. Plant Cell. 2011;23:701–715. doi: 10.1105/tpc.110.080788. PubMed DOI PMC

Song S., Huang H., Wang J., Liu B., Qi T., Xie D. MYC5 is involved in jasmonate-regulated plant growth, leaf senescence and defense responses. Plant Cell Physiol. 2017;58:1752–1763. doi: 10.1093/pcp/pcx112. PubMed DOI

Xu L. De novo root regeneration from leaf explants: Wounding, auxin, and cell fate transition. Curr. Opin. Plant Biol. 2018;41:39–45. doi: 10.1016/j.pbi.2017.08.004. PubMed DOI

Toyota M., Spencer D., Sawai-toyota S., Jiaqi W., Zhang T., Koo A.J., Howe G.A., Gilroy S. Glutamate triggers long-distance, calcium-based plant defense signaling. Science. 2018;6:1112–1115. doi: 10.1126/science.aat7744. PubMed DOI

Halliday K.J., Martinez-Garcia J.F., Josse E.M.J. Integration of light and auxin signaling. Cold Spring Harb. Perspect. Biol. 2009:1–12. doi: 10.1101/cshperspect.a001586. PubMed DOI PMC

Oh E., Zhu J.Y., Bai M.Y., Arenhart R.A., Sun Y., Wang Z.Y. Cell elongation is regulated through a central circuit of interacting transcription factors in the Arabidopsis hypocotyl. eLife. 2014;3:1–19. doi: 10.7554/eLife.03031. PubMed DOI PMC

Pacurar D.I., Pacurar M.L., Lakehal A., Pacurar A.M., Ranjan A., Bellini C. The Arabidopsis Cop9 signalosome subunit 4 (CSN4) is involved in adventitious root formation. Sci. Rep. 2017;7:1–12. PubMed PMC

Pacurar D.I., Pacurar M.L., Bussell J.D., Schwambach J., Pop T.I., Kowalczyk M., Gutierrez L., Cavel E., Chaabouni S., Ljung K., et al. Identification of new adventitious rooting mutants amongst suppressors of the Arabidopsis thaliana superroot2 mutation. J. Exp. Bot. 2014;65:1605–1618. doi: 10.1093/jxb/eru026. PubMed DOI PMC

Lorenzo O., Chico J., Sánchez-Serran J., Solano R. JASMONATE-INSENSITIVE1 Encodes a MYC Transcription Factor Essential to Discriminate between Different Jasmonate-Regulated Defense Responses in Arabidopsis. Plant Cell. 2004;16:1938–1950. doi: 10.1105/tpc.022319. PubMed DOI PMC

Ellis C., Turner J.G. A conditionally fertile coi1 allele indicates cross-talk between plant hormone signalling pathways in Arabidopsis thaliana seeds and young seedlings. Planta. 2002;215:549–556. doi: 10.1007/s00425-002-0787-4. PubMed DOI

Estelle M.A., Somerville C. Auxin-resistant mutants of Arabidopsis thaliana with an altered morphology. Mol. Gen. Genet. 1987;206:200–206. doi: 10.1007/BF00333575. DOI

Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., Preibisch S., Rueden C., Saalfeld S., Schmid B., et al. Fiji: An open-source platform for biological-image analysis. Nat. Methods. 2012;9:676–682. doi: 10.1038/nmeth.2019. PubMed DOI PMC

Xing H.L., Wang Z.P., Zhang H.Y., Han C.Y., Liu B., Wang X.C., Chen Q.J., Dong L. A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol. 2014;14:372. doi: 10.1186/s12870-014-0327-y. PubMed DOI PMC

Wang Z.P., Xing H.L., Dong L., Zhang H.Y., Han C.Y., Wang X.C., Chen Q.J. Egg cell-specific promoter-controlled CRISPR/Cas9 efficiently generates homozygous mutants for multiple target genes in Arabidopsis in a single generation. Genome Biol. 2015;16:1–12. doi: 10.1186/s13059-015-0715-0. PubMed DOI PMC

Floková K., Tarkowská D., Miersch O., Strnad M., Wasternack C., Novák O. UHPLC-MS/MS based target profiling of stress-induced phytohormones. Phytochemistry. 2014;105:147–157. doi: 10.1016/j.phytochem.2014.05.015. PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace