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

Zheping Yu, Yuying Ren, Jianwei Liu, Jian-Kang Zhu, Chunzhao Zhao

Stress Biology ›› 2022, Vol. 2 ›› Issue (1) : 13. DOI: 10.1007/s44154-022-00036-3
Original Paper

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

Author information +
History +

Abstract

Maintenance 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.

Keywords

Salt stress / Auxin / Reactive oxygen species / Plant cell wall / Arabidopsis

Cite this article

Download citation ▾
Zheping Yu, Yuying Ren, Jianwei Liu, Jian-Kang Zhu, Chunzhao Zhao. A novel mitochondrial protein is required for cell wall integrity, auxin accumulation and root elongation in Arabidopsis under salt stress. Stress Biology, 2022, 2(1): 13 https://doi.org/10.1007/s44154-022-00036-3

References

[1]
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
[2]
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
[4]
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.
[3]
CramerGR, EpsteinE, AndréL. Effects of sodium, potassium and calcium on salt-stressed barley. I. Growth analysis. Physiol Plant, 1990, 80(1):83-88
CrossRef Google scholar
[5]
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
[6]
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
[7]
DraegerC, Ndinyanka FabriceT, GineauE, MouilleG, KuhnBM, MollerI, AbdouMT, FreyB, PaulyM, BacicA, RingliC. Arabidopsis leucine-rich repeat extensin (LRX) proteins modify cell wall composition and influence plant growth. BMC Plant Biol, 2015, 15: 155
CrossRef Google scholar
[8]
EndlerA, KestenC, SchneiderR, ZhangY, IvakovA, FroehlichA, FunkeN, PerssonS. A mechanism for sustained cellulose synthesis during salt stress. Cell, 2015, 162(6):1353-1364
CrossRef Google scholar
[9]
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
[10]
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
[11]
FrimlJ, VietenA, SauerM, WeijersD, SchwarzH, HamannT, OffringaR, JürgensG. Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature, 2003, 426(6963):147-153
CrossRef Google scholar
[12]
FuY, YangY, ChenS, NingN, HuH. Arabidopsis IAR4 modulates primary root growth under salt stress through ROS-mediated modulation of auxin distribution. Front Plant Sci, 2019, 10: 522
CrossRef Google scholar
[13]
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
[14]
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
[15]
GeniselM, ErdalS, KızılkayaM. 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, 2014, 75(1):187-197
CrossRef Google scholar
[16]
GibeautDM, CarpitaNC. Tracing cell wall biogenesis in intact cells and plants: selective turnover and alteration of soluble and cell wall polysaccharides in grasses. Plant Physiol, 1991, 97(2):551-561
CrossRef Google scholar
[17]
GolldackD, LiC, MohanH, ProbstN. Tolerance to drought and salt stress in plants: unraveling the signaling networks. Front Plant Sci, 2014, 5: 151
CrossRef Google scholar
[18]
GongZH, XiongLM, ShiHZ, YangSH, LuisRE, XuGH, ChaoDY, LiJR, WangPC, QinF, LiJJ, DingYL, ShiYT, WangY, YangYQ, GuoY, ZhuJK. Plant abiotic stress response and nutrient use efficiency. Sci China Life Sci, 2020, 63(5):635-674
CrossRef Google scholar
[19]
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
[20]
HasegawaPM, BressanRA, ZhuJ-K, BohnertHJ. Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol, 2000, 51(1):463-499
CrossRef Google scholar
[21]
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
[22]
HuH, BrownPH. 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, 1994, 105(2):681-689
CrossRef Google scholar
[23]
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
[24]
LinCC, KaoCH. Proline accumulation is associated with inhibition of rice seedling root growth caused by NaCl. Plant Sci, 1996, 114(2):121-128
CrossRef Google scholar
[25]
LinCC, KaoCH. Cell wall peroxidase activity, hydrogen peroxide level and NaCl-inhibited root growth of rice seedlings. Plant Soil, 2001, 230(1):135-143
CrossRef Google scholar
[26]
LiuPR, WuWH. Physiological mechanisms of growth inhibition by concentrated potassium in Dunaliella Salina. J Integr Plant Biol, 1999, 41(6):617-623 https://www.jipb.net/EN/Y1999/V41/I6/
[27]
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
[28]
MalamyJE, RyanKS. Environmental regulation of lateral root initiation in Arabidopsis. Plant Physiol, 2001, 127(3):899-909
CrossRef Google scholar
[29]
MatchT. Boron in plant cell walls. Plant Soil, 1997, 193: 59-70
CrossRef Google scholar
[30]
McNeilM, DarvillAG, FrySC, AlbersheimP. Structure and function of the primary cell walls of plants. Annu Rev Biochem, 1984, 53(1):625-663
CrossRef Google scholar
[31]
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
[32]
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
[33]
O'NeillMA, EberhardS, AlbersheimP, DarvillAG. Requirement of borate cross-linking of cell wall rhamnogalacturonan II for Arabidopsis growth. Science, 2001, 294(5543):846-849
CrossRef Google scholar
[34]
O'NeillMA, IshiiT, AlbersheimP, DarvillAG. Rhamnogalacturonan II: structure and function of a borate cross-linked cell wall pectic polysaccharide. Annu Rev Plant Biol, 2004, 55(1):109-139
CrossRef Google scholar
[35]
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
[36]
PhangTH, ShaoG, LamHM. Salt tolerance in soybean. J Integr Plant Biol, 2008, 50(10):1196-1212
CrossRef Google scholar
[37]
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
[38]
RanochaP, DimaO, NagyR, FeltenJ, Corratgé-FaillieC, NovákO, MorreelK, LacombeB, MartinezY, PfrunderS, JinX, RenouJP, ThibaudJB, LjungK, FischerU, MartinoiaE, BoerjanW, GoffnerD. Arabidopsis WAT1 is a vacuolar auxin transport facilitator required for auxin homoeostasis. Nat Commun, 2013, 4(1):2625
CrossRef Google scholar
[39]
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
[40]
RodriguezHG, RobertsJ, JordanWR, DrewMC. Growth, water relations, and accumulation of organic and inorganic solutes in roots of maize seedlings during salt stress. Plant Physiol, 1997, 113(3):881-893
CrossRef Google scholar
[41]
RoySJ, NegrãoS, TesterM. Salt resistant crop plants. Curr Opin Biotechnol, 2014, 26: 115-124
CrossRef Google scholar
[42]
SheldenMC, RoessnerU. Advances in functional genomics for investigating salinity stress tolerance mechanisms in cereals. Front Plant Sci, 2013, 4: 123
CrossRef Google scholar
[43]
ShiH, KimY, GuoY, StevensonB, ZhuJK. The Arabidopsis SOS5 locus encodes a putative cell surface adhesion protein and is required for normal cell expansion. Plant Cell, 2003, 15(1):19-32
CrossRef Google scholar
[44]
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
[45]
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
[46]
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
[47]
WolfS, HématyK, HöfteH. Growth control and cell wall signaling in plants. Annu Rev Plant Biol, 2012, 63(1):381-407
CrossRef Google scholar
[48]
WuSJ, DingL, ZhuJK. SOS1, a genetic locus essential for salt tolerance and potassium acquisition. Plant Cell, 1996, 8(4):617-627
CrossRef Google scholar
[49]
YangL, ZhangJ, HeJ, QinY, HuaD, DuanY, ChenZ, GongZ. ABA-mediated ROS in mitochondria regulate root meristem activity by controlling PLETHORA expression in Arabidopsis. PLoS Genet, 2014, 10(12):e1004791
CrossRef Google scholar
[50]
YangY, GuoY. Unraveling salt stress signaling in plants. J Integr Plant Biol, 2018, 60(9):796-804
CrossRef Google scholar
[51]
YaoSX, ChenSS, XuDS, LanHY. Plant growth and responses of antioxidants of Chenopodium album to long-term NaCl and KCl stress. Plant Growth Regul, 2010, 60(2):115-125
CrossRef Google scholar
[52]
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
[53]
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
[54]
ZhaoKF, FanH, HarrisPJC. The physiological basis of growth inhibition of halophytes by potassium. J Integr Plant Biol, 1995, 37(6):437-442 https://www.jipb.net/EN/Y1995/V37/I6/
[55]
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
[56]
ZhuJ, FuX, KooYD, ZhuJK, JenneyFE Jr, AdamsMW, ZhuY, ShiH, YunDJ, HasegawaPM, BressanRA. An enhancer mutant of Arabidopsis salt overly sensitive 3 mediates both ion homeostasis and the oxidative stress response. Mol Cell Biol, 2007, 27(14):5214-5224
CrossRef Google scholar
[57]
ZhuJ, LeeBH, DellingerM, CuiX, ZhangC, WuS, NothnagelEA, ZhuJK. A cellulose synthase-like protein is required for osmotic stress tolerance in Arabidopsis. Plant J, 2010, 63(1):128-140
CrossRef Google scholar
[58]
ZhuJK. Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol, 2003, 6(5):441-445
CrossRef Google scholar
Funding
Shanghai Pujiang Program(20PJ1414800); National Natural Science Foundation of China(32070295); Strategic Priority Research Program of Chinese Academy of Sciences(XDB27040101); Shanghai Agriculture Applied Technology Development Program(G2020-01-01)

Accesses

Citations

Detail

Sections
Recommended

/