Interplay Between Proline Metabolism and ROS in the Fine Tuning of Root-Meristem Size in

Overview

Journal Plants (Basel)

Date 2022 Jun 10

PMID 35684285

Authors

Sara Bauduin

Martina Latini

Irene Belleggia

Marta Migliore

Marco Biancucci

Roberto Mattioli

Antonio Francioso

Luciana Mosca

Dietmar Funck

Maurizio Trovato

Affiliations

Soon will be listed here.

Abstract

We previously reported that proline modulates root meristem size in by controlling the ratio between cell division and cell differentiation. Here, we show that proline metabolism affects the levels of superoxide anion (O) and hydrogen peroxide (HO), which, in turn, modulate root meristem size and root elongation. We found that hydrogen peroxide plays a major role in proline-mediated root elongation, and its effects largely overlap those induced by proline, influencing root meristem size, root elongation, and cell cycle. Though a combination of genetic and pharmacological evidence, we showed that the short-root phenotype of the proline-deficient , an mutant homozygous for and heterozygous for , is caused by HO accumulation and is fully rescued by an effective HO scavenger. Furthermore, by studying mutants devoid of ProDH activity, we disclosed the essential role of this enzyme in the modulation of root meristem size as the main enzyme responsible for HO production during proline degradation. Proline itself, on the contrary, may not be able to directly control the levels of HO, although it seems able to enhance the enzymatic activity of catalase (CAT) and ascorbate peroxidase (APX), the two most effective scavengers of HO in plant cells. We propose a model in which proline metabolism participates in a delicate antioxidant network to balance HO formation and degradation and fine-tune root meristem size in .

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References

Choi W, Miller G, Wallace I, Harper J, Mittler R, Gilroy S . Orchestrating rapid long-distance signaling in plants with Ca , ROS and electrical signals. Plant J. 2017; 90(4):698-707. PMC: 5677518. DOI: 10.1111/tpj.13492. View

Hoque M, Banu M, Nakamura Y, Shimoishi Y, Murata Y . Proline and glycinebetaine enhance antioxidant defense and methylglyoxal detoxification systems and reduce NaCl-induced damage in cultured tobacco cells. J Plant Physiol. 2007; 165(8):813-24. DOI: 10.1016/j.jplph.2007.07.013. View

Nanjo T, Kobayashi M, Yoshiba Y, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K . Antisense suppression of proline degradation improves tolerance to freezing and salinity in Arabidopsis thaliana. FEBS Lett. 1999; 461(3):205-10. DOI: 10.1016/s0014-5793(99)01451-9. View

Dello Ioio R, Linhares F, Scacchi E, Casamitjana-Martinez E, Heidstra R, Costantino P . Cytokinins determine Arabidopsis root-meristem size by controlling cell differentiation. Curr Biol. 2007; 17(8):678-82. DOI: 10.1016/j.cub.2007.02.047. View

Saradhi P, Alia , Arora S, Prasad K . Proline accumulates in plants exposed to UV radiation and protects them against UV induced peroxidation. Biochem Biophys Res Commun. 1995; 209(1):1-5. DOI: 10.1006/bbrc.1995.1461. View

Khatun M, Matsushima D, Rhaman M, Okuma E, Nakamura T, Nakamura Y . Exogenous proline enhances antioxidant enzyme activities but does not mitigate growth inhibition by selenate stress in tobacco BY-2 cells. Biosci Biotechnol Biochem. 2020; 84(11):2281-2292. DOI: 10.1080/09168451.2020.1799747. View

Shinohara H, Mori A, Yasue N, Sumida K, Matsubayashi Y . Identification of three LRR-RKs involved in perception of root meristem growth factor in Arabidopsis. Proc Natl Acad Sci U S A. 2016; 113(14):3897-902. PMC: 4833249. DOI: 10.1073/pnas.1522639113. View

Yang S, Lan S, Gong M . Hydrogen peroxide-induced proline and metabolic pathway of its accumulation in maize seedlings. J Plant Physiol. 2009; 166(15):1694-9. DOI: 10.1016/j.jplph.2009.04.006. View

Verslues , Sharp . Proline accumulation in maize (Zea mays L.) primary roots at low water potentials. II. Metabolic source of increased proline deposition in the elongation zone . Plant Physiol. 1999; 119(4):1349-60. PMC: 32020. DOI: 10.1104/pp.119.4.1349. View

10.

Pan H, Guan D, Liu X, Li J, Wang L, Wu J . SIRT6 safeguards human mesenchymal stem cells from oxidative stress by coactivating NRF2. Cell Res. 2016; 26(2):190-205. PMC: 4746611. DOI: 10.1038/cr.2016.4. View

11.

Nomura M, Takagi H . Role of the yeast acetyltransferase Mpr1 in oxidative stress: regulation of oxygen reactive species caused by a toxic proline catabolism intermediate. Proc Natl Acad Sci U S A. 2004; 101(34):12616-21. PMC: 515106. DOI: 10.1073/pnas.0403349101. View

12.

Trovato M, Mattioli R, Costantino P . From RolD to Plant P5CS: Exploiting Proline to Control Plant Development. Plants (Basel). 2018; 7(4). PMC: 6313920. DOI: 10.3390/plants7040108. View

13.

Zhang X, Wang L, Xu X, Cai C, Guo W . Genome-wide identification of mitogen-activated protein kinase gene family in Gossypium raimondii and the function of their corresponding orthologs in tetraploid cultivated cotton. BMC Plant Biol. 2014; 14:345. PMC: 4270029. DOI: 10.1186/s12870-014-0345-9. View

14.

Moubayidin L, Perilli S, Dello Ioio R, Di Mambro R, Costantino P, Sabatini S . The rate of cell differentiation controls the Arabidopsis root meristem growth phase. Curr Biol. 2010; 20(12):1138-43. DOI: 10.1016/j.cub.2010.05.035. View

15.

Rentel M, Lecourieux D, Ouaked F, Usher S, Petersen L, Okamoto H . OXI1 kinase is necessary for oxidative burst-mediated signalling in Arabidopsis. Nature. 2004; 427(6977):858-61. DOI: 10.1038/nature02353. View

16.

Ma F, Wang L, Li J, Samma M, Xie Y, Wang R . Interaction between HY1 and H2O2 in auxin-induced lateral root formation in Arabidopsis. Plant Mol Biol. 2013; 85(1-2):49-61. DOI: 10.1007/s11103-013-0168-3. View

17.

Zafra A, Rejon J, Hiscock S, de Dios Alche J . Patterns of ROS Accumulation in the Stigmas of Angiosperms and Visions into Their Multi-Functionality in Plant Reproduction. Front Plant Sci. 2016; 7:1112. PMC: 4974276. DOI: 10.3389/fpls.2016.01112. View

18.

Dunand C, Crevecoeur M, Penel C . Distribution of superoxide and hydrogen peroxide in Arabidopsis root and their influence on root development: possible interaction with peroxidases. New Phytol. 2007; 174(2):332-341. DOI: 10.1111/j.1469-8137.2007.01995.x. View

19.

Fabro G, Kovacs I, Pavet V, Szabados L, Alvarez M . Proline accumulation and AtP5CS2 gene activation are induced by plant-pathogen incompatible interactions in Arabidopsis. Mol Plant Microbe Interact. 2004; 17(4):343-50. DOI: 10.1094/MPMI.2004.17.4.343. View

20.

Hasanuzzaman M, Bhuyan M, Zulfiqar F, Raza A, Mohsin S, Mahmud J . Reactive Oxygen Species and Antioxidant Defense in Plants under Abiotic Stress: Revisiting the Crucial Role of a Universal Defense Regulator. Antioxidants (Basel). 2020; 9(8). PMC: 7465626. DOI: 10.3390/antiox9080681. View