Abstract
Main conclusion
Auxin acts upstream of NO through NOA and XXT5 pathways to regulate the binding capacity of the root cell wall to Al.
Abstract
In our previous study, we identified an unknown mechanism by which 1-naphthaleneacetic acid (NAA) decreased the fixation of aluminum (Al) in the cell wall. Here, we observed that external application of the nitric oxide (NO) donor S-nitrosoglutathion (GSNO) increased the inhibition of Al on root elongation. Further analysis indicated that GSNO could induce Al accumulation in the roots and root cell walls, which is consistent with lower xyloglucan content. In comparison to the Columbia-0 (Col-0) wild type (WT), endogenous NO-reduced mutants noa1 (NOA pathway) and nia1nia2 (NR pathway) were more resistant to Al, with lower root Al content, higher xyloglucan content, and more Al accumulation in the root cell walls. By contrast, the xxt5 mutant with reduced xyloglucan content exhibited an Al-sensitive phenotype. Interestingly, Al treatment increased the endogenous auxin and NO levels, and the auxin levels induced under Al stress further stimulated NO production. Auxin application reduced Al retention in hemicellulose and decreased the xyloglucan content, similar to the effects observed with GSNO. In yucca and aux1-7 mutants, exogenous application of NO resulted in responses similar to those of the WT, whereas exogenous auxin had little effect on the noa1 mutant under Al stress. In addition, as auxin had similar effects on the nia1nia2 mutant and the WT, exogenous auxin and NO had little effect on the xxt5 mutant under Al stress, further confirming that auxin acts upstream of NO through NOA and XXT5 pathways to regulate the binding capacity of the root cell wall to Al.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The data that has been used is confidential.
Abbreviations
- ALS1:
-
Aluminum sensitive 1
- GSNO:
-
S-nitrosoglutathion
- L-NAME:
-
Nw-nitro-l-Arg-methylester
- NAA:
-
1-Naphthaleneacetic acid
- NO:
-
Nitric oxide
- NOA:
-
Nitric oxide-associated
- NR:
-
Nitrate reductase
- XXT:
-
Xyloglucan xylosyltransferase
References
Ahn SJ, Rengel Z, Matsumoto H (2003) Aluminum-induced plasma membrane surface potential and H+-ATPase activity in near-isogenic wheat lines differing in tolerance to aluminum. New Phytol 162:71–79. https://doi.org/10.1111/j.1469-8137.2004.01009.x
Barcelo J, Poschenrieder C (2002) Fast root growth responses, root exudates, and internal detoxification as clues to the mechanisms of aluminum toxicity and resistance: a review. Environ Exp Bot 48:75–92. https://doi.org/10.1016/s0098-8472(02)00013-8
Besson-Bard A, Pugin A, Wendehenne D (2008) New insights into nitric oxide signaling in plants. Annu Rev Plant Biol 59:21–23. https://doi.org/10.1146/annurev.arplant.59.032607.092830
Cavalier DM, Lerouxel O, Neumetzler L, Yamauchi K, Reinecke A, Freshour G, Zabotina OA, Hahn MG, Burgert I, Pauly M, Raikhel NV, Keegstra K (2008) Disrupting two Arabidopsis thaliana xylosyltransferase genes results in plants deficient in xyloglucan, a major primary cell wall component. Plant Cell 20:1519–1537. https://doi.org/10.1105/tpc.108.059873
Chang YC, Yamamoto Y, Matsumoto H (1999) Accumulation of aluminium in the cell wall pectin in cultured tobacco (Nicotiana tabacum L.) cells treated with a combination of aluminium and iron. Plant Cell Environ 22:1009–1017. https://doi.org/10.1046/j.1365-3040.1999.00467.x
Chen WW, Yang JL, Qin C, Jin CW, Mo JH, Ye T, Zheng SJ (2010) Nitric oxide acts downstream of auxin to trigger root ferric-chelate reductase activity in response to iron deficiency in Arabidopsis thaliana. Plant Physiol 154:810–819. https://doi.org/10.1104/pp.110.161109
Doncheva S, Amenos M, Poschenrieder C, Barcelo J (2005) Root cell patterning: a primary target for aluminium toxicity in maize. J Exp Bot 56:1213–1220. https://doi.org/10.1093/jxb/eri115
Du ST, Zhang YS, Lin XY, Wang Y, Tang CX (2008) Regulation of nitrate reductase by its partial product nitric oxide in Chinese cabbage pakchoi (Brassica chinensis L. cv. Baoda). Plant Cell Environ 31:195–204. https://doi.org/10.1111/j.1365-3040.2007.01750.x
Hagen G, Guilfoyle T (2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Mol Biol Rep 49:373–385. https://doi.org/10.1007/978-94-010-0377-3_9
He HY, He LF, Gu MH, Li XF (2012) Nitric oxide improves aluminum tolerance by regulating hormonal equilibrium in the root apices of rye and wheat. Plant Sci 183:123–130. https://doi.org/10.1016/j.plantsci.2011.07.012
Kochian LV (1995) Cellular mechanisms of aluminum toxicity and resistance in plants. Annu Rev Plant Physiol Mol Biol 46:237–260. https://doi.org/10.1146/annurev.pp.46.060195.001321
Kollmeier M, Felle HH, Horst WJ (2000) Genotypical differences in aluminum resistance of maize are expressed in the distal part of the transition zone. Is reduced basipetalauxin flow involved in inhibition of root elongation by aluminum? Plant Physiol 122:945–956. https://doi.org/10.1104/pp.122.3.945
Labavitch JM (1981) Cell wall turnover in plant development. Annu Rev Plant Physiol 32:385–406. https://doi.org/10.1146/annurev.pp.32.060181.002125
Labavitch JM, Ray PM (1974) Turnover of cell wall polysaccharides in elongating pea stem segments. Plant Physiol 53:669–673. https://doi.org/10.1104/pp.53.5.669
Leitner M, Vandelle E, Gaupels F, Bellin D, Delledonne M (2009) NO signals in the haze: nitric oxide signalling in plant defence. Curr Opin Plant Biol 12:451–458
Liu J, Piñeros MA, Kochian LV (2014) The role of aluminum sensing and signaling in plant aluminum resistance. J Integr Plant Biol 56:221–230. https://doi.org/10.1016/j.pbi.2009.05.012
Ljung K, Hull AK, Celenza J, Yamada M, Estelle M, Normanly J, Sandberg G (2005) Sites and regulation of auxin biosynthesis in Arabidopsis roots. Plant Cell 17:1090–1104. https://doi.org/10.1105/tpc.104.029272
Madson M, Dunand C, Li X, Verma R, Vanzin GF, DA CaplanJ S, Carpita NC, Reiter WD (2003) The MUR3 gene of Arabidopsis encodes a xyloglucan galactosyltransferase that is evolutionarily related to animal exostosins. Plant Cell 15:1662–1670. https://doi.org/10.1105/tpc.009837
Matsumoto H (2000) Cell biology of aluminum toxicity and tolerance in higher plants. Int Rev Cytol 200:1–46. https://doi.org/10.1016/s0074-7696(00)00001-2
Neill SJ, Desikan R, Hancock JT (2003) Nitric oxide signaling in plants. New Phytol 159:11–35
Nishitani K, Masuda Y (1981) Auxin-induced changes in the cell wall structure: changes in the sugar compositions, intrinsic viscosity and molecular weight distribution of matrix polysaccharides of the epicotyl cell wall of Vigna angularis. Physiol Plant 52:482–494. https://doi.org/10.1111/j.1399-3054.1981.tb02720.x
Pacheco-Villalobos D, Diaz-Moreno SM, van der Schuren A, Tamaki T, Kang YH, Gujas B, Novak O, Jaspert N, Li ZN, Wolf S, Oecking C, Ljung K, Bulone V, Hardtke CS (2016) The effects of high steady state auxin levels on root cell elongation in Brachypodium. Plant Cell 28:1009–1024. https://doi.org/10.1105/tpc.15.01057
Stamler JS, Loscalzo J (1992) Capillary zone electrophoretic detection of biological thiols and their S-nitrosated derivatives. Anal Chem 64:779–785. https://doi.org/10.1021/ac00031a014
Sun P, Tian QY, Jie C, Zhang WH (2010) Aluminium-induced inhibition of root elongation in Arabidopsis is mediated by ethylene and auxin. J Exp Bot 61:347–356. https://doi.org/10.1093/jxb/erp306
Sun CL, Lu LL, Liu LJ, Liu WJ, Yu Y, Liu XX, Hu Y, Jin CW, Lin XY (2014) Nitrate reductase-mediated early nitric oxide burst alleviates oxidative damage induced by aluminum through enhancement of antioxidant defenses in roots of wheat (Triticum aestivum). New Phytol 201:1240–1250. https://doi.org/10.1111/nph.12597
Tabuchi A, Matsumoto H (2001) Changes in cell-wall properties of wheat (Triticum aestivum) roots during aluminum-induced growth inhibition. Physiol Plant 112:353–358. https://doi.org/10.1034/j.1399-3054.2001.1120308.x
Tao Y, Wan JX, Liu YS, Yang XZ, Shen RF, Zhu XF (2022) The NAC transcription factor ANAC017 regulates aluminum tolerance by regulating the cell wall-modifying genes. Plant Physiol 189:2517–2534. https://doi.org/10.1093/plphys/kiac197
Taylor GJ, McDonald-Stephens JL, Hunter DB, Bertsch PM, Elmore D, Rengel Z, Reid RJ (2000) Direct measurement of aluminum uptake and distribution in single cells of Chara corallina. Plant Physiol 123:987–996. https://doi.org/10.1104/pp.123.3.987
Terry ME, Bonner BA (1980) An examination of centrifugation as a model of extracting an extracellular solution from peas and its use for the study of IAA-induced growth. Plant Physiol 66:321–325. https://doi.org/10.1104/pp.66.2.321
Tian QY, Sun DH, Zhao MG, Zhang WH (2007) Inhibition of nitric oxide synthase (NOS) underlies aluminum-induced inhibition of root elongation in Hibiscus moscheutos. New Phytol 174:322–331. https://doi.org/10.1111/j.1469-8137.2007.02005.x
Wang YS, Yang ZM (2005) Nitric oxide reduces aluminum toxicity by preventing oxidative stress in the roots of Cassia tora L. Plant Cell Physiol 46:1915–1923. https://doi.org/10.1093/pcp/pci202
Wang HH, Huang JJ, Bi YR (2010) Nitrate reductase-dependent nitric oxide production is involved in aluminum tolerance in red kidney bean roots. Plant Sci 179:281–288. https://doi.org/10.1016/j.plantsci.2010.05.014
Wang HH, Huang JJ, Liang WH, Liang XL, Bi YR (2013) Involvement of putrescine and nitric oxide in aluminum tolerance by modulating citrate secretion from roots of red kidney bean. Plant Soil 366:479–490. https://doi.org/10.1007/s11104-012-1447-5
Wu Q, Tao Y, Huang J, Liu YS, Yang XZ, Jing HK, Shen RF, Zhu XF (2022) The MYB transcription factor MYB103 acts upstream of TRICHOME BIREFRINGENCE-LIKE27 in regulating aluminum sensitivity by modulating the O-acetylation level of cell wall xyloglucan in Arabidopsis thaliana. Plant J 111:529–545. https://doi.org/10.1111/tpj.15837
Yang JL, Li YY, Zhang YJ, Zhang SS, Wu YR, Zheng SJ (2008) Cell wall polysaccharides are specifically involved in the exclusion of aluminum from the rice root apex. Plant Physiol 146:602–611. https://doi.org/10.1104/pp.107.111989
Yang JL, Zhu XF, Zheng C, Zhang YJ, Zheng SJ (2011) Genotypic differences in Al resistance and the role of cell-wall pectin in Al exclusion from root apex in Fagopyrum tataricum. Ann Bot-London 107:371–378. https://doi.org/10.1093/aob/mcq254
Yang L, Tian D, Todd CD, Luo Y, Hu X (2013) Comparative proteome analyses reveal that nitric oxide is an important signal molecule in the response of rice to aluminum toxicity. J Proteome Res 12:1316–1330. https://doi.org/10.1021/pr300971n
Yang ZB, Geng X, He C, Zhang F, Wang R, Horst WJ, Ding Z (2014) TAA1-regulated local auxin biosynthesis in the root-apex transition zone mediates the aluminum-induced inhibition of root growth in Arabidopsis. Plant Cell 26:2889–2904. https://doi.org/10.1105/tpc.114.127993
Zabotina OA, van de Ven WTG, Freshour G, Drakakaki G, Cavalier D, Mouille G, Hahn MG, Keegstra K, Raikhel NV (2008) Arabidopsis XXT5 gene encodes a putative a-1,6-xylosyltransferase that is involved in xyloglucan biosynthesis. Plant J 56:101–115. https://doi.org/10.1111/j.1365-313x.2008.03580.x
Zhang SJ, Song XQ, Yua BS, Zhang BC, Sun CQ, Knox JP, Zhou YH (2012) Identification of quantitative trait loci affecting hemicellulose characteristics based on cell wall composition in a wild and cultivated rice species. Mol Plant 5:162–175. https://doi.org/10.1093/mp/ssr076
Zheng SJ, Lin XY, Yang JL, Liu Q, Tang CX (2004) The kinetics of aluminum adsorption and desorptiion by root cell walls of an aluminum resistant wheat (Triticum aestivum L.) cultivar. Plant Soil 261:85–90. https://doi.org/10.1023/b:plso.0000035576.71760.2b
Zhou Y, Xu XY, Chen LQ, Yang JL, Zheng SJ (2012) Nitric oxide exacerbates Al-induced inhibition of root elongation in rice bean by affecting cell wall and plasma membrane properties. Phytochem Lett 76:46–51. https://doi.org/10.1016/j.phytochem.2011.12.004
Zhu XF, Shi YZ, Lei GJ, Fry SC, Zhang BC, Zhou YH, Braam J, Jiang T, Xu XY, Mao CZ, Pan YJ, Yang JL, Wu P, Zheng SJ (2012) XTH31, encoding an in-vitro XEH/XET-active enzyme, controls Al sensitivity by modulating in-vivo XET action, cell wall xyloglucan content and Al binding capacity in Arabidopsis. Plant Cell 24:4731–4747. https://doi.org/10.1105/tpc.112.106039
Zhu XF, Lei GJ, Wang ZW, Shi YZ, Braam J, Li GX, Zheng SJ (2013) Coordination between apoplastic and symplastic detoxification confers plant Al resistance. Plant Physiol 162:1947–1955. https://doi.org/10.1104/pp.113.219147
Zhu XF, Sun Y, Zhang BC, Mansoori N, Wan JX, Liu Y, Wang ZW, Shi YZ, Zhou YH, Zheng SJ (2014a) TRICHOME BIREFRIGENCE-LIKE27 affects aluminum sensitivity by modulating the O-acetylation of xyloglucan and aluminum-binding capacity in Arabidopsis. Plant Physiol 166:181–189. https://doi.org/10.1104/pp.114.243808
Zhu XF, Wan JX, Sun Y, Shi YZ, Braam J, Li GX, Zheng SJ (2014b) Xyloglucan endotransglucosylase-hydrolase17 interacts with xyloglucan endotransglucosylase-hydrolase31 to confer xyloglucan endotransglucosylase action and affect aluminum sensitivity in Arabidopsis. Plant Physiol 165:1566–1574. https://doi.org/10.1104/pp.114.243790
Zhu XF, Wan JX, Wu Q, Zhao XS, Zheng SJ, Shen RF (2017) PARVUS affects aluminum sensitivity by modulating the structure of glucuronoxylan in Arabidopsis thaliana. Plant Cell Environ 40:1916–1925. https://doi.org/10.1111/pce.12999
Acknowledgements
This study was supported by the Foundation for Distinguished Young Scholars of Jiangsu Province, China [grant no. BK20190050] and the Youth Innovation Promotion Association of the Chinese Academy of Sciences [Grant No. 2015250]. We would like to thank Editage (www.editage.cn) for English language editing. Thanks are also given to the editor and the anonymous reviewer for their valuable comments to improve the quality of our work.
Author information
Authors and Affiliations
Contributions
XFZ and RFS designed the experiments; SL, JYS and HYW performed the experiments and analyzed the data; SL wrote the manuscript; HKJ and XFZ revised the manuscript. All authors have read and approved the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Communicated by Dorothea Bartels.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Li, S., Sun, J.Y., Wang, H.Y. et al. Auxin acts upstream of nitric oxide to regulate cell wall xyloglucan and its aluminium-binding capacity in Arabidopsis thaliana. Planta 259, 52 (2024). https://doi.org/10.1007/s00425-024-04331-3
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-024-04331-3