Hydrogen peroxide homeostasis provides beneficial micro-environment for SHR-mediated periclinal division in Arabidopsis root.
Arabidopsis
SHORT-ROOT (SHR)
hydrogen peroxide
micro-environment
periclinal division
reactive oxygen species (ROS)
root
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
12 2020
12 2020
Historique:
received:
02
06
2020
accepted:
13
07
2020
pubmed:
25
7
2020
medline:
15
5
2021
entrez:
25
7
2020
Statut:
ppublish
Résumé
The precise regulation of asymmetric cell division (ACD) is essential for plant organogenesis. In Arabidopsis roots, SHORT-ROOT (SHR) functions to promote periclinal division in cortex/endodermis initials, which generate the ground tissue patterning. Although multiple downstream transcription factors and interplaying hormone pathways have been reported, the cellular mechanism that affects SHR-mediated periclinal division remains largely unclear. Here, we found that SHR can substantially elevate reactive oxygen species (ROS) levels in Arabidopsis roots by activating respiratory burst oxidase homologs (RBOHs). Among the ROS products, hydrogen peroxide (H
Substances chimiques
Arabidopsis Proteins
0
SNC1 protein, Arabidopsis
0
Hydrogen Peroxide
BBX060AN9V
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1926-1938Informations de copyright
© 2020 The Authors New Phytologist © 2020 New Phytologist Trust.
Références
Alvarez ME, Pennell RI, Meijer PJ, Ishikawa A, Dixon RA, Lamb C. 1998. Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92: 773-784.
Baum SF, Dubrovsky JG, Rost TL. 2002. Apical organization and maturation of the cortex and vascular cylinder in Arabidopsis thaliana (Brassicaceae) roots. American Journal of Botany 89: 908-920.
Benjamini Y, Yekutieli D. 2001. The control of the false discovery rate in multiple testing under dependency. Annals of Statistics 29: 1165-1188.
Cao H, Bowling SA, Gordon S, Dong X. 1994. Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6: 1583-1592.
Chen Z, Silva H, Klessig DF. 1993. Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 262: 1883-1886.
Chin L, Yu J, Fu Y, Yu T, Liu A, Luo K. 2011. Production of reactive oxygen species in endothelial cells under different pulsatile shear stresses and glucose concentrations. Lab on a Chip 11: 1856-1863.
Conrath U, Chen Z, Ricigliano JR, Klessig DF. 1995. Two inducers of plant defense responses, 2,6-dichloroisonicotinec acid and salicylic acid, inhibit catalase activity in tobacco. Proceedings of the National Academy of Sciences, USA 92: 7143-7147.
Cui H, Kong D, Wei P, Hao Y, Torii KU, Lee JS, Li J. 2014. SPINDLY, ERECTA, and its ligand STOMAGEN have a role in redox-mediated cortex proliferation in the Arabidopsis root. Molecular Plant 7: 1727-1739.
Cui H, Levesque MP, Vernoux T, Jung JW, Paquette AJ, Gallagher KL, Wang JY, Blilou I, Scheres B, Benfey PN. 2007. An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 316: 421-425.
Dolan L, Janmaat K, Willemsen V, Linstead P, Poethig S, Roberts K, Scheres B. 1993. Cellular organization of the Arabidopsis thaliana root. Development 119: 71-84.
Falk A, Feys BJ, Frost LN, Jones JDG, Daniels MJ, Parker JE. 1999. EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. Proceedings of the National Academy of Sciences, USA 96: 3292-3297.
Gong X, Flores-Vergara MA, Hong JH, Chu H, Lim J, Franks RG, Liu Z, Xu J. 2016. SEUSS integrates gibberellin signaling with transcriptional inputs from the SHR-SCR-SCL3 module to regulate middle cortex formation in the Arabidopsis root. Plant Physiology 170: 1677-1683.
Hejátko J, Blilou I, Brewer PB, Friml J, Scheres B, Benková E. 2006. In situ hybridization technique for mRNA detection in whole mount Arabidopsis samples. Nature Protocols 1: 1939-1946.
Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Benfey PN. 2000. The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101: 555-567.
Heo JO, Chang KS, Kim IA, Lee MH, Lee SA, Song SK, Lee MM, Lim J. 2011. Funneling of gibberellin signaling by the GRAS transcription regulator SCARECROW-LIKE 3 in the Arabidopsis root. Proceedings of the National Academy of Sciences, USA 108: 2166-2171.
Hu Y, Liu S, Yuan H, Jing L, Yan D, Zhang JLuY. 2010. Functional comparison of catalase genes in the elimination of photorespiratory H2O2 using promoter- and 3′-untranslated region exchange experiments in the Arabidopsis cat2 photorespiratory mutant. Plant, Cell & Environment 33: 1656-1670.
Jirage D, Tootle TL, Reuber TL, Frost LN, Feys BJ, Parker JE, Ausubel FM, Glazebrook J. 1999. Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. Proceedings of the National Academy of Sciences, USA 96: 13583-13588.
Kaurilind E, Xu E, Brosché M. 2015. A genetic framework for H2O2 induced cell death in Arabidopsis thaliana. BMC Genomics 16: 837.
Klessig D, Choi H, Dempsey D. 2018. Systemic acquired resistance and salicylic acid: past, present and future. Molecular Plant-Microbe Interactions 31: 871-888.
Koizumi K, Hayashi T, Gallagher KL. 2012. SCARECROW reinforces SHORT-ROOT signaling and inhibits periclinal cell divisions in the ground tissue by maintaining SHR at high levels in the endodermis. Plant Signaling & Behavior 7: 1573-1577.
Lee SA, Jang S, Yoon EK, Heo JO, Chang KS, Choi JW, Dhar S, Kim G, Choe JE, Heo JB et al. 2016. Interplay between ABA and GA modulates the timing of asymmetric cell divisions in the Arabidopsis root ground tissue. Molecular Plant 9: 870-884.
Lee Y, Rubio MC, Alassimone J, Geldner N. 2013. A mechanism for localized lignin deposition in the endodermis. Cell 153: 402-412.
Li X, Clarke JD, Zhang Y, Dong X. 2001. Activation of an EDS1-mediated R-gene pathway in the snc1 mutant leads to constitutive, NPR1-independent pathogen resistance. Molecular Plant-Microbe Interactions 14: 1131-1139.
Li X, Zhang Y, Clarke JD, Li Y, Dong X. 1999. Identification and cloning of a negative regulator of systemic acquired resistance, SNI1, through a screen for suppressors of npr1-1. Cell 98: 329-339.
Long Y, Smet W, Cruz-Ramírez A, Castelijns B, de Jonge W, Mähönen AP, Bouchet BP, Perez GS, Akhmanova A, Scheres B. 2015. Arabidopsis BIRD zinc finger proteins jointly stabilize tissue boundaries by confining the cell fate regulator SHORT-ROOT and contributing to fate specification. Plant Cell 27: 1185-1199.
Marino D, Dunand C, Puppo A, Pauly N. 2012. A burst of plant NADPH oxidases. Trends in Plant Science 17: 9-15.
Mittler R. 2017. ROS are good. Trends in Plant Science 22: 11-19.
Nakajima K, Sena G, Nawy T, Benfey PN. 2001. Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413: 307-311.
Olszewski NE, West CM, Sassi SO, Hartweck LM. 2010. O-GlcNAc protein modification in plants: evolution and function. Biochimica et Biophysica Acta-General Subjects 1800: 49-56.
Paquette AJ, Benfey PN. 2005. Maturation of the ground tissue of the root is regulated by gibberellin and SCARECROW and requires SHORT-ROOT. Plant Physiology 138: 636-640.
Pasternak T, Groot EP, Kazantsev FV, Teale W, Omelyanchuk N, Kovrizhnykh V, Palme K, Mironova VV. 2019. Salicylic acid affects root meristem patterning via auxin distribution in a concentration-dependent manner. Plant Physiology 180: 1725-1739.
Robinson MD, McCarthy DJ, Smyth GK. 2010. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Biogeoences 26: 139-140.
Rustérucci C, Aviv DH, Holt BF III, Dangl JL, Parker JE. 2001. The disease resistance signaling components EDS1 and PAD4 are essential regulators of the cell death pathway controlled by LSD1 in Arabidopsis. Plant Cell 13: 2211-2224.
Sena G, Jung JW, Benfey PN. 2004. A broad competence to respond to SHORT ROOT revealed by tissue-specific ectopic expression. Development 131: 2817-2826.
Shah J, Chaturvedi R, Chowdhury Z, Venables B, Petros RA. 2014. Signaling by small metabolites in systemic acquired resistance. The Plant Journal 79: 645-658.
Shapiguzov A, Vainonen JP, Wrzaczek M, Kangasjärvi J. 2012. ROS-talk - how the apoplast, the chloroplast, and the nucleus get the message through. Frontiers Plant Science 3: 1-9.
Sozzani R, Cui H, Moreno-Risueno MA, Busch W, Van Norman JM, Vernoux T, Brady SM, Dewitte W, Murray JAH, Benfey PN. 2010. Spatiotemporal regulation of cell-cycle genes by SHORTROOT links patterning and growth. Nature 466: 128-132.
Strimmer K. 2008. A unified approach to false discovery rate estimation. BMC Bioinformatics 9: 303.
Tian Y, Fan M, Qin Z, Lv H, Wang M, Zhang Z, Zhou W, Zhao N, Li X, Han C et al. 2018. Hydrogen peroxide positively regulates brassinosteroid signaling through oxidation of the BRASSINAZOLE-RESISTANT1 transcription factor. Nature Communications 9: 1063.
Tsukagoshi H, Busch W, Benfey PN. 2010. Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143: 606-616.
van den Berg C, Weisbeek P, Scheres B. 1998. Cell fate and cell differentiation status in the Arabidopsis root. Planta 205: 483-491.
Walker KL, Muller S, Moss D, Ehrhardt DW, Smith LG. 2007. Arabidopsis TANGLED identifies the division plane throughout mitosis and cytokinesis. Current Biology 17: 1827-1836.
Waszczak C, Kerchev PI, Mühlenbock P, Hoeberichts FA, Van Der Kelen K, Mhamdi A, Willems P, Denecker J, Kumpf RP, Noctor G et al. 2016. SHORT-ROOT deficiency alleviates the cell death phenotype of the Arabidopsis catalase2 mutant under photorespiration-promoting conditions. Plant Cell 28: 1844-1859.
Yamada M, Han X, Benfey PN. 2020. RGF1 controls root meristem size through ROS signalling. Nature 577: 85-88.
Yang L, Zhang J, He J, Qin Y, Hua D, Duan Y, Chen Z, Gong Z. 2014. ABA-mediated ROS in mitochondria regulate root meristem activity by controlling PLETHORA expression in Arabidopsis. PLoS Genetics 10: e1004791.
Yu Q, Li P, Liang N, Wang H, Wu S. 2017. Cell-fate specification in Arabidopsis roots requires coordinative action of lineage instruction and positional reprogramming. Plant Physiology 175: 816-827.
Yu Q, Tian H, Yue K, Liu J, Zhang B, Li X, Ding Z. 2016. A P-Loop NTPase regulates quiescent center cell division and distal stem cell identity through the regulation of ROS homeostasis in Arabidopsis root. PLoS Genetics 12: e1006175.
Yuan HM, Liu WC, Lu YT. 2017. CATALASE2 coordinates SA-mediated repression of both auxin accumulation and JA biosynthesis in plant defenses. Cell Host & Microbe 21: 143-155.
Zeng J, Dong Z, Wu H, Tian Z, Zhao Z. 2017. Redox regulation of plant stem cell fate. EMBO Journal 36: 2844-2855.
Zhang J, Kirkham MB. 1996. Lipid peroxidation in sorghum and sunflower seedlings as affected by ascorbic acid, benzoic acid, and propyl gallate. Journal of Plant Physiology 149: 489-493.
Zhang X, Henriques R, Lin SS, Niu QW, Chua NH. 2006. Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nature Protocols 1: 641-646.