Modified Crosstalk between Phytohormones in Arabidopsis Mutants for PEP-Associated Proteins

. 2024 Jan 27 ; 25 (3) : . [epub] 20240127

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid38338865

Grantová podpora
122042700044-6 Grant from the state assignment of the Ministry of Science and Higher Education of the Russian Federation

Plastid-encoded RNA polymerase (PEP) forms a multisubunit complex in operating chloroplasts, where PEP subunits and a sigma factor are tightly associated with 12 additional nuclear-encoded proteins. Mutants with disrupted genes encoding PEP-associated proteins (PAPs) provide unique tools for deciphering mutual relationships among phytohormones. A block of chloroplast biogenesis in Arabidopsis pap mutants specifying highly altered metabolism in white tissues induced dramatic fluctuations in the content of major phytohormones and their metabolic genes, whereas hormone signaling circuits mostly remained functional. Reprogramming of the expression of biosynthetic and metabolic genes contributed to a greatly increased content of salicylic acid (SA) and a concomitant decrease in 1-aminocyclopropane-1-carboxylic acid (ACC) and oxophytodienoic acid (OPDA), precursors of ethylene and jasmonic acid, respectively, in parallel to reduced levels of abscisic acid (ABA). The lack of differences in the free levels of indole-3-acetic acid (IAA) between the pap mutants and wild-type plants was accompanied by fluctuations in the contents of IAA precursors and conjugated forms as well as multilayered changes in the expression of IAA metabolic genes. Along with cytokinin (CK) overproduction, all of these compensatory changes aim to balance plant growth and defense systems to ensure viability under highly modulated conditions.

Zobrazit více v PubMed

Robles P., Quesada V. Research Progress in the Molecular Functions of Plant mTERF Proteins. Cells. 2021;10:205. doi: 10.3390/cells10020205. PubMed DOI PMC

Börner T., Aleynikova A.Y., Zubo Y.O., Kusnetsov V.V. Chloroplast RNA polymerases: Role in chloroplast biogenesis. Biochim. Biophys. Acta. 2015;1847:761–769. doi: 10.1016/j.bbabio.2015.02.004. PubMed DOI

Liebers M., Pfannschmidt T. Plastid RNA polymerases and nuclear-encoded proteins associated with them in Arabidopsis thaliana. Endocytobiosis Cell Res. 2017;28:20–32.

Pfannschmidt T., Blanvillain R., Merendino L., Courtois F., Chevalier F., Liebers M., Lerbs-Mache S. Plastid RNA polymerases: Orchestration of enzymes with different evolutionary origins controls chloroplast biogenesis during the plant life cycle. J. Exp. Bot. 2015;66:6957–6973. doi: 10.1093/jxb/erv415. PubMed DOI

Grübler B., Merendino L., Twardziok S.O., Mininno M., Allorent G., Chevalier F., Ravanel S. Light and plastid signals regulate different sets of genes in the albino mutant pap7-1. Plant Physiol. 2017;175:1203–1219. doi: 10.1104/pp.17.00982. PubMed DOI PMC

Grübler B., Cozzi C., Pfannschmidt T. A Core Module of Nuclear Genes Regulated by Biogenic Retrograde Signals from Plastids. Plants. 2021;10:296. doi: 10.3390/plants10020296. PubMed DOI PMC

Danilova M.N., Andreeva A.A., Doroshenko A.S., Kudryakova N.V., Kuznetsov V.V., Kusnetsov V.V. Phytohormones Regulate the Expression of Nuclear Genes Encoding the Components of the Plastid Transcription Apparatus. Dokl. Biochem. Biophys. 2018;478:25–29. doi: 10.1134/S1607672918010076. PubMed DOI

Andreeva A.A., Vankova R., Bychkov I.A., Kudryakova N.V., Danilova M.N., Lacek J., Pojidaeva E.S., Kusnetsov V.V. Cytokinin-Regulated Expression of Arabidopsis thaliana PAP Genes and Its Implication for the Expression of Chloroplast-Encoded Genes. Biomolecules. 2020;10:1658. doi: 10.3390/biom10121658. PubMed DOI PMC

Nemhauser J.L., Hong F., Chory J. Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell. 2006;126:467–475. doi: 10.1016/j.cell.2006.05.050. PubMed DOI

Yagi Y., Ishizaki Y., Nakahira Y., Tozawa Y., Shiina T. Eukaryotic-type plastid nucleoid protein pTAC3 is essential for transcription by the bacterial-type plastid RNA polymerase. Proc. Natl. Acad. Sci. USA. 2012;109:7541–7546. doi: 10.1073/pnas.1119403109. PubMed DOI PMC

Arsova B., Hoja U., Wimmelbacher M., Greiner E., Üstün Ş., Melzer M., Börnke F. Plastidial thioredoxin z interacts with two fructokinase-like proteins in a thiol-dependent manner: Evidence for an essential role in chloroplast development in Arabidopsis and Nicotiana benthamiana. Plant Cell. 2010;22:1498–1515. doi: 10.1105/tpc.109.071001. PubMed DOI PMC

Gilkerson J., Perez-Ruiz J.M., Chory J., Callis J. The plastid-localized pfkB-type carbohydrate kinases FRUCTOKINASE-LIKE 1 and 2 are essential for growth and development of Arabidopsis thaliana. BMC Plant Biol. 2012;12:102. doi: 10.1186/1471-2229-12-102. PubMed DOI PMC

Korasick D.A., Enders T.A., Strader L.C. Auxin biosynthesis and storage forms. J. Exp. Bot. 2013;64:2541–2555. doi: 10.1093/jxb/ert080. PubMed DOI PMC

Cohen J.D., Bandurski R.S. Chemistry and Physiology of the bound auxin. Ann. Rev. Plant Physiol. 1982;33:403–430. doi: 10.1146/annurev.pp.33.060182.002155. DOI

Leon-Reyes A., Van der Does D., De Lange E.S., Delker C., Wasternack C., Van Wees S.C., Ritsema T., Pieterse C.M. Salicylate-mediated suppression of jasmonate-responsive gene expression in Arabidopsis is targeted downstream of the jasmonate biosynthesis pathway. Planta. 2010;232:1423–1432. doi: 10.1007/s00425-010-1265-z. PubMed DOI PMC

Gawroński P., Górecka M., Bederska M., Rusaczonek A., Slesak I., Kruk J., Karpiński S. Isochorismate synthase 1 is required for thylakoid organization, optimal plastoquinone redox status, and state transitions in Arabidopsis thaliana. J. Exp. Bot. 2013;64:3669–3679. doi: 10.1093/jxb/ert203. PubMed DOI PMC

Li N., Han X., Feng D., Yuan D., Huang L.-J. Signaling Crosstalk between Salicylic Acid and Ethylene/Jasmonate in Plant Defense: Do We Understand What They Are Whispering? Int. J. Mol. Sci. 2019;20:671. doi: 10.3390/ijms20030671. PubMed DOI PMC

Wu Y., Zhang D., Yan Chu J., Boyle P., Wang Y., Brindle I.D., De Luca V., Despre’s C. The Arabidopsis NPR1 Protein Is a Receptor for the Plant Defense Hormone Salicylic Acid. Cell Rep. 2012;1:639–647. doi: 10.1016/j.celrep.2012.05.008. PubMed DOI

Zhong Q., Hu H., Fan B., Zhu C., Chen Z. Biosynthesis and Roles of Salicylic Acid in Balancing Stress Response and Growth in Plants. Int. J. Mol. Sci. 2021;22:11672. doi: 10.3390/ijms222111672. PubMed DOI PMC

Wang D., Pajerowska-Mukhtar K., Culler A.H., Dong X. Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Curr. Biol. 2007;17:1784–1790. doi: 10.1016/j.cub.2007.09.025. PubMed DOI

Kong W., Li Y., Zhang M., Jin F., Li J. A Novel Arabidopsis MicroRNA Promotes IAA Biosynthesis via the Indole-3-acetaldoxime Pathway by Suppressing SUPERROOT1. Plant Cell Physiol. 2015;56:715–726. doi: 10.1093/pcp/pcu216. PubMed DOI

Guo R., Hu Y., Aoi Y., Hira H., Ge C., Dai X., Kasahara H., Zhao Y. Local conjugation of auxin by the GH3 amido synthetases is required for normal development of roots and flowers in Arabidopsis. Biochem. Biophys. Res. Commun. 2022;589:16–22. doi: 10.1016/j.bbrc.2021.11.109. PubMed DOI

Pattyn J., Vaughan-Hirsch J., Van de Poel B. The regulation of ethylene biosynthesis: A complex multilevel control circuitry. New Phytol. 2021;229:770–782. doi: 10.1111/nph.16873. PubMed DOI PMC

Oñate-Sánchez L., Anderson J.P., Young J., Singh K.B. AtERF14, a Member of the ERF Family of Transcription Factors, Plays a Nonredundant Role in Plant Defense. Plant Physiol. 2007;143:400–409. doi: 10.1104/pp.106.086637. PubMed DOI PMC

Cheng M.-C., Liao P.-M., Kuo W.-W., Lin T.-P. The Arabidopsis ETHYLENE RESPONSE FACTOR1 Regulates Abiotic Stress-Responsive Gene Expression by Binding to Different cis-Acting Elements in Response to Different Stress Signals. Plant Physiol. 2013;162:1566–1582. doi: 10.1104/pp.113.221911. PubMed DOI PMC

Dong Z., Yu Y., Li S., Wang J., Tang S., Huang R. Abscisic Acid Antagonizes Ethylene Production through the ABI4-Mediated Transcriptional Repression of ACS4 and ACS8 in Arabidopsis. Mol. Plant. 2016;9:126–135. doi: 10.1016/j.molp.2015.09.007. PubMed DOI

Singh A., Roychoudhury A. Abscisic acid in plants under abiotic stress: Crosstalk with major phytohormones. Plant Cell Rep. 2023;42:961–974. doi: 10.1007/s00299-023-03013-w. PubMed DOI

Danilova M.N., Kudryakova N.V., Doroshenko A.S., Zabrodin D.A., Rakhmankulova Z.F., Oelmüller R., Kusnetsov V.V. Opposite roles of the Arabidopsis cytokinin receptors AHK2 and AHK3 in the expression of plastid genes and genes for the plastid transcriptional machinery during senescence. Plant Mol. Biol. 2017;93:533–546. doi: 10.1007/s11103-016-0580-6. PubMed DOI

Wang Y., Chang H.P., Hu S., Lu X.T., Yuan C.Y., Zhang C., Wang P., Xiao W.J., Xiao L.T., Xue G.P., et al. Plastid casein kinase 2 knockout reduces abscisic acid (ABA) sensitivity, thermotolerance, and expression of ABA and heat stress responsive nuclear genes. J. Exp. Bot. 2014;65:4159–4175. doi: 10.1093/jxb/eru190. PubMed DOI PMC

Yamburenko M.V., Zubo Y.O., Börner T. Abscisic acid affects transcription of chloroplast genes via protein phosphatase 2C-dependent activation of nuclear genes: Repression by guanosine-3′-5′-bisdiphosphate and activation by sigma factor 5. Plant J. 2015;82:1030–1041. doi: 10.1111/tpj.12876. PubMed DOI

Aluru M.R., Zola J., Foudree A., Rodermel S.R. Chloroplast Photooxidation-Induced Transcriptome Reprogramming in Arabidopsis immutans White Leaf Sectors. Plant Physiol. 2009;150:904–923. doi: 10.1104/pp.109.135780. PubMed DOI PMC

Pogorelko G.V., Kambakam S., Nolan T., Foudree A., Zabotina O.A., Rodermel S.R. Impaired Chloroplast Biogenesis in Immutans, an Arabidopsis Variegation Mutant, Modifies Developmental Programming, Cell Wall Composition and Resistance to Pseudomonas syringae. PLoS ONE. 2016;1:e0150983. doi: 10.1371/journal.pone.0150983. PubMed DOI PMC

Hirosawa Y., Tada A., Matsuura T., Mori I.C., Ogura Y., Hayashi T., Uehara S., Ito-Inaba Y., Inaba T. Salicylic Acid Acts Antagonistically to Plastid Retrograde Signaling by Promoting the Accumulation of Photosynthesis-associated Proteins in Arabidopsis. Plant Cell Physiol. 2021;62:1728–1744. doi: 10.1093/pcp/pcab128. PubMed DOI

Kurepin L.V., Ivanov A.G., Zaman M., Pharis R.P., Allakhverdiev S.I., Hurry V., Hüner P.A. Stress-related hormones and glycinebetaine interplayin protection of photosynthesis under abiotic stress conditions. Photosyn. Res. 2015;126:221–235. doi: 10.1007/s11120-015-0125-x. PubMed DOI

Choi J., Huh S.U., Mikiko Kojima M., Sakakibara H., Paek K.-H., Hwang I. The Cytokinin-Activated Transcription Factor ARR2 Promotes Plant Immunity via TGA3/NPR1-Dependent Salicylic Acid Signaling in Arabidopsis Developmental. Cell. 2010;19:284–295. doi: 10.1016/j.devcel.2010.07.011. PubMed DOI

Mothes K., Engelbrecht L., Schűtte H.R. Ǘber den Akkumulationvon α- minoisobuttersaure im Blatgewebe unter dem Einfluss von Kinetin. Physiol. Plant. 1961;14:72–76. doi: 10.1111/j.1399-3054.1961.tb08139.x. DOI

Mothes K., Engelbrecht L. On the activity of a kinetin-like root factor. Life Sci. 1963;11:852–857. doi: 10.1016/0024-3205(63)90098-5. DOI

Dobrev P.I., Kamınek M. Fast and efficient separation of cytokinins from auxin and abscisic acid and their purification using mixed-mode solid-phase extraction. J. Chromatogr. A. 2002;950:21–29. doi: 10.1016/S0021-9673(02)00024-9. PubMed DOI

Dobrev P.I., Vankova R. Quantification of abscisic acid, cytokinin, and auxin content in salt-stressed plant tissues. Methods Mol. Biol. 2012;913:251–261. doi: 10.1007/978-1-61779-986-0_17. PubMed DOI

Bychkov I.A., Andreeva A.A., Kudryakova N.V., Pojidaeva E.S., Kusnetsov V.V. The role of PAP4/FSD3 and PAP9/FSD2 in heat stress responses of chloroplast genes. Plant Sci. 2022;322:111359. doi: 10.1016/j.plantsci.2022.111359. PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...