A novel mitochondrial protein is required for cell wall integrity, auxin accumulation and root elongation in Arabidopsis under salt stress

Zheping Yu1, Yuying Ren2, Jianwei Liu2, Jian‐Kang Zhu2, Chunzhao Zhao2
1Institute of Horticulture, Zhejiang Academy of Agricultural Sciences, Hangzhou, China
2Shanghai Center for Plant Stress Biology, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences, Shanghai, China

Tóm tắt

AbstractMaintenance of root elongation is beneficial for the growth and survival of plants under salt stress, but currently the cellular components involved in the regulation of root growth under high salinity are not fully understood. In this study, we identified an Arabidopsis mutant, rres1, which exhibited reduced root elongation under treatment of a variety of salts, including NaCl, NaNO3, KCl, and KNO3. RRES1 encodes a novel mitochondrial protein and its molecular function is still unknown. Under salt stress, the root meristem length was shorter in the rres1 mutant compared to the wild type, which was correlated with a reduced auxin accumulation in the mutant. Reactive oxygen species (ROS), as important signals that regulate root elongation, were accumulated to higher levels in the rres1 mutant than the wild type after salt treatment. Measurement of monosaccharides in the cell wall showed that arabinose and xylose contents were decreased in the rres1 mutant under salt stress, and application of boric acid, which is required for the crosslinking of pectic polysaccharide rhamnogalacturonan-II (RG-II), largely rescued the root growth arrest of the rres1 mutant, suggesting that RRES1 participates in the maintenance of cell wall integrity under salt stress. GUS staining assay indicated that the RRES1 gene was expressed in leaves and weakly in root tip under normal conditions, but its expression was dramatically increased in leaves and roots after salt treatment. Together, our study reveals a novel mitochondrial protein that regulates root elongation under salt stress via the modulation of cell wall integrity, auxin accumulation, and ROS homeostasis.

Từ khóa


Tài liệu tham khảo

Burget EG, Reiter WD (1999) The mur4 mutant of Arabidopsis is partially defective in the de novo synthesis of uridine diphospho L-arabinose. Plant Physiol 121(2):383–389. https://doi.org/10.1104/pp.121.2.383

Burget EG, Verma R, Mølhøj M, Reiter WD (2003) The biosynthesis of L-arabinose in plants: molecular cloning and characterization of a Golgi-localized UDP-D-xylose 4-epimerase encoded by the MUR4 gene of Arabidopsis. Plant Cell 15(2):523–531. https://doi.org/10.1105/tpc.008425

Christian G, David K, Domenica H, Rolf B, Jörg K, Ralf RM, Robert H (2011) Quantitative analysis of dynamic protein-protein interactions in planta by a floated-leaf luciferase complementation imaging (FLuCI) assay using binary Gateway vectors.  Plant J 67(3):542–553. https://doi.org/10.1111/j.1365-313X.2011.04607.x.

Cramer GR, Epstein E, André L (1990) Effects of sodium, potassium and calcium on salt-stressed barley. I. Growth analysis. Physiol Plant 80(1):83–88. https://doi.org/10.1111/j.1399-3054.1990.tb04378.x

Dello LR, Linhares FS, Scacchi E, Casamitjana-Martinez E, Heidstra R, Costantino P, Sabatini S (2007) Cytokinins determine Arabidopsis root-meristem size by controlling cell differentiation. Curr Biol 17(8):678–682. https://doi.org/10.1016/j.cub.2007.02.047

Deslauriers SD, Larsen PB (2010) FERONIA is a key modulator of brassinosteroid and ethylene responsiveness in Arabidopsis hypocotyls. Mol Plant 3(3):626–640. https://doi.org/10.1093/mp/ssq015

Draeger C, Ndinyanka Fabrice T, Gineau E, Mouille G, Kuhn BM, Moller I, Abdou MT, Frey B, Pauly M, Bacic A, Ringli C (2015) Arabidopsis leucine-rich repeat extensin (LRX) proteins modify cell wall composition and influence plant growth. BMC Plant Biol 15:155. https://doi.org/10.1186/s12870-015-0548-8

Endler A, Kesten C, Schneider R, Zhang Y, Ivakov A, Froehlich A, Funke N, Persson S (2015) A mechanism for sustained cellulose synthesis during salt stress. Cell 162(6):1353–1364. https://doi.org/10.1016/j.cell.2015.08.028

Eshel A (1985) Response of Suaeda aegyptiaca to KCl, NaCl and Na2SO4 treatments. Physiol Plant 64(3):308–315. https://doi.org/10.1111/j.1399-3054.1985.tb03345.x

Feng W, Kita D, Peaucelle A, Cartwright HN, Doan V, Duan Q, Liu MC, Maman J, Steinhorst L, Schmitz-Thom I, Yvon R, Kudla J, Wu HM, Cheung AY, Dinneny JR (2018) The FERONIA receptor kinase maintains Cell-Wall integrity during salt stress through Ca2+ signaling. Curr Biol 28(5):666–675.e5. https://doi.org/10.1016/j.cub.2018.01.023

Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jürgens G (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426(6963):147–153. https://doi.org/10.1038/nature02085

Fu Y, Yang Y, Chen S, Ning N, Hu H (2019) Arabidopsis IAR4 modulates primary root growth under salt stress through ROS-mediated modulation of auxin distribution. Front Plant Sci 10:522. https://doi.org/10.3389/fpls.2019.00522

Fujii H, Verslues PE, Zhu JK (2011) Arabidopsis decuple mutant reveals the importance of SnRK2 kinases in osmotic stress responses in vivo. Proc Natl Acad Sci U S A 108(4):1717–1722. https://doi.org/10.1073/pnas.1018367108

Galvan-Ampudia CS, Testerink C (2011) Salt stress signals shape the plant root. Curr Opin Plant Biol 14(3):296–302. https://doi.org/10.1016/j.pbi.2011.03.019

Genisel M, Erdal S, Kızılkaya M (2014) The mitigating effect of cysteine on growth inhibition in salt-stressed barley seeds is related to its own reducing capacity rather than its effects on antioxidant system. Plant Growth Regul 75(1):187–197. https://doi.org/10.1007/s10725-014-9943-7

Gibeaut DM, Carpita NC (1991) Tracing cell wall biogenesis in intact cells and plants: selective turnover and alteration of soluble and cell wall polysaccharides in grasses. Plant Physiol 97(2):551–561. https://doi.org/10.1104/pp.97.2.551

Golldack D, Li C, Mohan H, Probst N (2014) Tolerance to drought and salt stress in plants: unraveling the signaling networks. Front Plant Sci 5:151. https://doi.org/10.3389/fpls.2014.00151

Gong ZH, Xiong LM, Shi HZ, Yang SH, Luis RE, Xu GH, Chao DY, Li JR, Wang PC, Qin F, Li JJ, Ding YL, Shi YT, Wang Y, Yang YQ, Guo Y, Zhu JK (2020) Plant abiotic stress response and nutrient use efficiency. Sci China Life Sci 63(5):635–674. https://doi.org/10.1007/s11427-020-1683-x

Harholt J, Suttangkakul A, Vibe Scheller H (2010) Biosynthesis of pectin. Plant Physiol 153(2):384–395. https://doi.org/10.1104/pp.110.156588

Hasegawa PM, Bressan RA, Zhu J-K, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51(1):463–499. https://doi.org/10.1146/annurev.arplant.51.1.463

Hazman M, Hause B, Eiche E, Nick P, Riemann M (2015) Increased tolerance to salt stress in OPDA-deficient rice ALLENE OXIDE CYCLASE mutants is linked with an increased ROS-scavenging activity. J Exp Bot 66(11):3339–3352. https://doi.org/10.1093/jxb/erv142

Hu H, Brown PH (1994) Localization of boron in cell walls of squash and tobacco and its association with pectin (evidence for a structural role of boron in the Cell Wall). Plant Physiol 105(2):681–689. https://doi.org/10.1104/pp.105.2.681

Hu R, Zhu Y, Wei J, Chen J, Shi H, Shen G, Zhang H (2017) Overexpression of PP2A-C5 that encodes the catalytic subunit 5 of protein phosphatase 2A in Arabidopsis confers better root and shoot development under salt conditions. Plant Cell Environ 40(1):150–164. https://doi.org/10.1111/pce.12837

Lin CC, Kao CH (1996) Proline accumulation is associated with inhibition of rice seedling root growth caused by NaCl. Plant Sci 114(2):121–128. https://doi.org/10.1016/0168-9452(96)04323-3

Lin CC, Kao CH (2001) Cell wall peroxidase activity, hydrogen peroxide level and NaCl-inhibited root growth of rice seedlings. Plant Soil 230(1):135–143. https://doi.org/10.1023/A:1004876712476

Liu PR, Wu WH (1999) Physiological mechanisms of growth inhibition by concentrated potassium in Dunaliella Salina. J Integr Plant Biol 41(6):617–623 https://www.jipb.net/EN/Y1999/V41/I6/

Liu W, Li RJ, Han TT, Cai W, Fu ZW, Lu YT (2015) Salt stress reduces root meristem size by nitric oxide-mediated modulation of auxin accumulation and signaling in Arabidopsis. Plant Physiol 168(1):343–356. https://doi.org/10.1104/pp.15.00030

Malamy JE, Ryan KS (2001) Environmental regulation of lateral root initiation in Arabidopsis. Plant Physiol 127(3):899–909. https://doi.org/10.1104/pp.127.3.899

Match T (1997) Boron in plant cell walls. Plant Soil 193:59–70. https://doi.org/10.1023/A:1004207824251

McNeil M, Darvill AG, Fry SC, Albersheim P (1984) Structure and function of the primary cell walls of plants. Annu Rev Biochem 53(1):625–663. https://doi.org/10.1146/annurev.bi.53.070184.003205

Mertz RA, Olek AT, Carpita NC (2012) Alterations in cell-wall glycosyl linkage structure of Arabidopsis murus mutants. Carbohydr Polym 89(2):331–339. https://doi.org/10.1016/j.carbpol.2012.02.044

Moldovan L, Moldovan NI (2004) Oxygen free radicals and redox biology of organelles. Histochem Cell Biol 122(4):395–412. https://doi.org/10.1007/s00418-004-0676-y

O'Neill MA, Eberhard S, Albersheim P, Darvill AG (2001) Requirement of borate cross-linking of cell wall rhamnogalacturonan II for Arabidopsis growth. Science 294(5543):846–849. https://doi.org/10.1126/science.1062319

O'Neill MA, Ishii T, Albersheim P, Darvill AG (2004) Rhamnogalacturonan II: structure and function of a borate cross-linked cell wall pectic polysaccharide. Annu Rev Plant Biol 55(1):109–139. https://doi.org/10.1146/annurev.arplant.55.031903.141750

Petricka JJ, Winter CM, Benfey PN (2012) Control of Arabidopsis root development. Annu Rev Plant Biol 63(1):563–590. https://doi.org/10.1146/annurev-arplant-042811-105501

Phang TH, Shao G, Lam HM (2008) Salt tolerance in soybean. J Integr Plant Biol 50(10):1196–1212. https://doi.org/10.1111/j.1744-7909.2008.00760.x

Rahnama A, Munns R, Poustini K, Watt M (2011) A screening method to identify genetic variation in root growth response to a salinity gradient. J Exp Bot 62(1):69–77. https://doi.org/10.1093/jxb/erq359

Ranocha P, Dima O, Nagy R, Felten J, Corratgé-Faillie C, Novák O, Morreel K, Lacombe B, Martinez Y, Pfrunder S, Jin X, Renou JP, Thibaud JB, Ljung K, Fischer U, Martinoia E, Boerjan W, Goffner D (2013) Arabidopsis WAT1 is a vacuolar auxin transport facilitator required for auxin homoeostasis. Nat Commun 4(1):2625. https://doi.org/10.1038/ncomms3625

Tomas R, Fernanda GV, Antonio OJ (2020) Auxin-mediated responses under salt stress: from developmental regulation to biotechnological applications. J Exp Bot 71(13):3843–3853. https://doi.org/10.1093/jxb/eraa241

Rodriguez HG, Roberts J, Jordan WR, Drew MC (1997) Growth, water relations, and accumulation of organic and inorganic solutes in roots of maize seedlings during salt stress. Plant Physiol 113(3):881–893. https://doi.org/10.1104/pp.113.3.881

Roy SJ, Negrão S, Tester M (2014) Salt resistant crop plants. Curr Opin Biotechnol 26:115–124. https://doi.org/10.1016/j.copbio.2013.12.004

Shelden MC, Roessner U (2013) Advances in functional genomics for investigating salinity stress tolerance mechanisms in cereals. Front Plant Sci 4:123. https://doi.org/10.3389/fpls.2013.00123

Shi H, Kim Y, Guo Y, Stevenson B, Zhu JK (2003) The Arabidopsis SOS5 locus encodes a putative cell surface adhesion protein and is required for normal cell expansion. Plant Cell 15(1):19–32. https://doi.org/10.1105/tpc.007872

Suzuki N, Koussevitzky S, Mittler R, Miller G (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 35(2):259–270. https://doi.org/10.1111/j.1365-3040.2011.02336.x

Tsukagoshi H (2012) Defective root growth triggered by oxidative stress is controlled through the expression of cell cycle-related genes. Plant Sci 197:30–39. https://doi.org/10.1016/j.plantsci.2012.08.011

Wang Y, Li K, Li X (2009) Auxin redistribution modulates plastic development of root system architecture under salt stress in Arabidopsis thaliana. J Plant Physiol 166(15):1637–1645. https://doi.org/10.1016/j.jplph.2009.04.009

Wolf S, Hématy K, Höfte H (2012) Growth control and cell wall signaling in plants. Annu Rev Plant Biol 63(1):381–407. https://doi.org/10.1146/annurev-arplant-042811-105449

Wu SJ, Ding L, Zhu JK (1996) SOS1, a genetic locus essential for salt tolerance and potassium acquisition. Plant Cell 8(4):617–627. https://doi.org/10.1105/tpc.8.4.617

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 Genet 10(12):e1004791. https://doi.org/10.1371/journal.pgen.1004791

Yang Y, Guo Y (2018) Unraveling salt stress signaling in plants. J Integr Plant Biol 60(9):796–804. https://doi.org/10.1111/jipb.12689

Yao SX, Chen SS, Xu DS, Lan HY (2010) Plant growth and responses of antioxidants of Chenopodium album to long-term NaCl and KCl stress. Plant Growth Regul 60(2):115–125. https://doi.org/10.1007/s10725-009-9426-4

Yuan HM, Xu HH, Liu WC, Lu YT (2013) Copper regulates primary root elongation through PIN1-mediated auxin redistribution. Plant Cell Physiol 54(5):766–778. https://doi.org/10.1093/pcp/pct030

Zhao C, Zayed O, Zeng F, Liu C, Zhang L, Zhu P, Hsu CC, Tuncil YE, Tao WA, Carpita NC, Zhu JK (2019) Arabinose biosynthesis is critical for salt stress tolerance in Arabidopsis. New Phytol 224(1):274–290. https://doi.org/10.1111/nph.15867

Zhao KF, Fan H, Harris PJC (1995) The physiological basis of growth inhibition of halophytes by potassium. J Integr Plant Biol 37(6):437–442 https://www.jipb.net/EN/Y1995/V37/I6/

Zhong H, LÄUchli A (1993) Spatial and temporal aspects of growth in the primary root of cotton seedlings: effects of NaCl and CaCl2. J Exp Bot 44:763–771. https://doi.org/10.1093/jxb/44.4.763

Zhu J, Fu X, Koo YD, Zhu JK, Jenney FE Jr, Adams MW, Zhu Y, Shi H, Yun DJ, Hasegawa PM, Bressan RA (2007) An enhancer mutant of Arabidopsis salt overly sensitive 3 mediates both ion homeostasis and the oxidative stress response. Mol Cell Biol 27(14):5214–5224. https://doi.org/10.1128/MCB.01989-06

Zhu J, Lee BH, Dellinger M, Cui X, Zhang C, Wu S, Nothnagel EA, Zhu JK (2010) A cellulose synthase-like protein is required for osmotic stress tolerance in Arabidopsis. Plant J 63(1):128–140. https://doi.org/10.1111/j.1365-313X.2010.04227.x

Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6(5):441–445. https://doi.org/10.1016/s1369-5266(03)00085-2