Cell wall pectin and its methyl-esterification in transition zone determine Al resistance in cultivars of pea (Pisum sativum)

Frontiers in Plant Science

Volumn 7, Issue FEB2016, 2016, Pages

  Li, Xuewen ^a,b   Li, Yalin ^a,b   Qu, Mei ^a,b   Xiao, Hongdong ^b   Feng, Yingming ^b   Liu, Jiayou ^b   Wu, Lishu ^a   Yu, Min ^b  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^b FOSHAN UNIVERSITY   (China)

Author keywords

Aluminum sensitivity; Cell wall pectin; Degree of pectin methyl esterification; Pea; Pectin methylesterase activity; Transition zone

Indexed keywords

EID: 84958542347     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2016.00039     Document Type: Article

References (51)

1. Anthon, G. E., and Barrett, D. M. (2004). Comparison of three colorimetric reagents in the determination of methanol with alcohol oxidase. Application to the assay of pectin methylesterase. J. Agric. Food Chem. 52, 3749-3753. doi: 10.1021/jf035284w.
2. Baluška, F., Barlow, P. W., and Kubica, Š. (1994). Importance of the post-mitotic isodiametric growth (PIG) region for growth and development of roots. Plant Soil 167, 31-41. doi: 10.1007/BF01587595.
3. Baluška, F., Volkmann, D., and Barlow, P. W. (1996). Specialized zones of development in roots: view from the cellular level. Plant Physiol. 112, 3-4.
4. Baluška, F., Volkmann, D., and Barlow, P. W. (2001). A polarity crossroad in the transition growth zone of maize root apices: cytoskeletal and developmental implications. J. Plant Growth Regul. 20, 170-181. doi: 10.1007/s003440010013.
5. Blamey, F. P. C., Asher, C. J., Edwards, D. C., and Kerven, G. L. (1993). In vitro evidence of aluminum effects on solution movement through root cell walls. J. Plant Nutr. 16, 555-562. doi: 10.1080/01904169309364556.
6. Blamey, F. P. C., Edmeades, D. C., and Wheeler, D. M. (1990). Role of root cation-exchange capacity in differential aluminum tolerance of Lotus species. J. Plant Nutr. 13, 729-744. doi: 10.1080/01904169009364112.
7. Blamey, F. P. C., Nishizawa, N. K., and Yoshimura, E. (2004). Timing, magnitude, and location of initial soluble aluminum injuries to mungbean roots. Soil Sci. Plant Nutr. 50, 67-76. doi: 10.1080/00380768.2004.10408453.
8. Blamey, F. P. C., Nishizawa, N. K., and Yoshimura, E. (2005). Digital microscopy: a useful technique for measuring root elongation in solution. Soil Sci. Plant Nutr. 51, 705-708. doi: 10.1111/j.1747-0765.2005.tb00096.x.
9. Blumenkrantz, N., and Asboe-Hansen, G. (1973). New method for quantitative determination of uronic acids. Anal. Biochem. 54, 484-489. doi: 10.1016/0003-2697(73)90377-1.
10. Chang, Y. C., Yamamoto, Y., and 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. doi: 10.1046/j.1365-3040.1999.00467.x.
11. Clarkson, D. T. (1967). Interactions between aluminium and phosphorus on root surfaces and cell wall material. Plant Soil 27, 347-356. doi: 10.1007/BF01376328.
12. Delhaize, E., and Ryan, P. R. (1995). Aluminum toxicity and tolerance in plants. Plant Physiol. 107, 315-321.
13. Eticha, D., Stass, A., and Horst, W. J. (2005a). Cell-wall pectin and its degree of methylation in the maize root-apex: significance for genotypic differences in aluminium resistance. Plant Cell Environ. 28, 1410-1420. doi: 10.1111/j.1365-3040.2005.01375.x.
14. Eticha, D., Staß, A., and Horst, W. J. (2005b). Localization of aluminium in the maize root apex: can morin detect cell wall-bound aluminium? J. Exp. Bot. 56, 1351-1357. doi: 10.1093/jxb/eri136.
15. Foy, C. D. (1988). Plant adaptation to acid, aluminum-toxic soils. Commun. Soil Sci. Plant Anal. 19, 959-987. doi: 10.1080/00103628809367988.
16. Heim, D. R., Skomp, J. R., Waldron, C., and Larrinua, I. M. (1991). Differential response to isoxaben of cellulose biosynthesis by wild-type and resistant strains of Arabidopsis thaliana. Pestic. Biochem. Physiol. 39, 93-99. doi: 10.1016/0048-3575(91)90129-A.
17. Horst W. J. (1995). Effect of aluminium on membrane properties of soybean (Glycine max) cells in suspension culture. Plant Soil 171, 113-118. doi: 10.1007/BF00009572.
18. Horst, W. J., Kollmeier, M., Schmohl, N., Sivaguru, M., Wang, Y., Felle, H. H., et al. (2007). "Significance of the root apoplast for aluminium toxicity and resistance of maize," in The Apoplast of Higher Plants: Compartment of Storage, Transport, and Reactions, eds B. Sattelmacher and W. J. Horst (Dordrecht: Springer).
19. Horst, W. J., Schmohl, N., Kollmeier, M., Balu Ka, F. E., and Sivaguru, M. (1999). Does aluminium affect root growth of maize through interaction with the cell wall-plasma membrane-cytoskeleton continuum? Plant Soil 215, 163-174. doi: 10.1023/A:1004439725283.
20. Horst, W. J., Wang, Y., and Eticha, D. (2010). The role of the root apoplast in aluminium-induced inhibition of root elongation and in aluminium resistance of plants: a review. Ann. Bot. 106, 185-197. doi: 10.1093/aob/mcq053.
21. Hoson, T., Soga, K., Wakabayashi, K., Kamisaka, S., and Tanimoto, E. (2003). "Growth and cell wall changes in rice roots during spaceflight," in Proceedings of the Roots: The Dynamic Interface between Plants and the Earth, ed. J. Abe (Nagoya: Springer), 19-26.
22. Huang, C., Yamaji, N., Chen, Z., and Ma, J. F. (2012). A tonoplast-localized half-size ABC transporter is required for internal detoxification of aluminum in rice. Plant J. 69, 857-867. doi: 10.1111/j.1365-313X.2011.04837.x.
23. Illéš, P., Schlicht, M., Pavlovkin, J., Lichtscheidl, I., Baluška, F., and Ovečka, M. (2006). Aluminium toxicity in plants: internalization of aluminium into cells of the transition zone in Arabidopsis root apices related to changes in plasma membrane potential, endosomal behaviour, and nitric oxide production. J. Exp. Bot. 57, 4201-4213. doi: 10.1093/jxb/erl197.
24. Jorge, R. A., and Arruda, P. (1997). Aluminum-induced organic acids exudation by roots of an aluminum-tolerant tropical maize. Phytochemistry 45, 675-681. doi: 10.1016/S0031-9422(97)00044-7.
25. Klug, B., Specht, A., and Horst, W. J. (2011). Aluminium localization in root tips of the aluminium-accumulating plant species buckwheat (Fagopyrum esculentum Moench).J. Exp. Bot. 62, 5453-5462. doi: 10.1093/jxb/err222.
26. Kobayashi, M., Mutoh, T., and Matoh, T. (2004). Boron nutrition of cultured tobacco BY-2 cells. IV. Genes induced under low boron supply. J. Exp. Bot. 55, 1441-1443. doi: 10.1093/jxb/erh142.
27. Kochian, L. V. (1995). Cellular mechanisms of aluminum toxicity and resistance in plants. Annu. Rev. Plant Biol. 46, 237-260. doi: 10.1146/annurev.pp.46.060195.001321.
28. Kollmeier, M., Felle, H. H., and Horst, W. J. (2000). Genotypical differences in aluminum resistance of maize are expressed in the distal part of the transition zone. Is reduced basipetal auxin flow involved in inhibition of root elongation by aluminum?Plant Physiol. 122, 945-956. doi: 10.1104/pp.122.3.945.
29. Kyomugasho, C., Christiaens, S., Shpigelman, A., Van Loey, A. M., and Hendrickx, M. E. (2015). FT-IR spectroscopy, a reliable method for routine analysis of the degree of methylesterification of pectin in different fruit-and vegetable-based matrices. Food Chem. 176, 82-90. doi: 10.1016/j.foodchem.2014.12.033.
30. Llugany, M., Poschenrieder, C., and Barceló, J. (1995). Monitoring of aluminium-induced inhibition of root elongation in four maize cultivars differing in tolerance to aluminium and proton toxicity. Physiol. Plant. 93, 265-271. doi: 10.1111/j.1399-3054.1995.tb02227.x.
31. Louvet, R., Rayon, C., Domon, J.-M., Rusterucci, C., Fournet, F., Leaustic, A., et al. (2011). Major changes in the cell wall during silique development in Arabidopsis thaliana. Phytochemistry 72, 59-67. doi: 10.1016/j.phytochem.2010.10.008.
32. Micheli, F. (2001). Pectin methylesterases: cell wall enzymes with important roles in plant physiology. Trends Plant Sci. 6, 414-419. doi: 10.1016/S1360-1385(01)02045-3.
33. Rangel, A. F., Rao, I. M., and Horst, W. J. (2007). Spatial aluminium sensitivity of root apices of two common bean (Phaseolus vulgaris L.) genotypes with contrasting aluminium resistance. J. Exp. Bot. 58, 3895-3904. doi: 10.1093/jxb/erm241.
34. Rangel, A. F., Rao, I. M., and Horst, W. J. (2009). Intracellular distribution and binding state of aluminum in root apices of two common bean (Phaseolus vulgaris) genotypes in relation to Al toxicity. Physiol. Plant. 135, 162-173. doi: 10.1111/j.1399-3054.2008.01183.x.
35. Rengel, Z., and Reid, R. J. (1997). Uptake of Al across the plasma membrane of plant cells. Plant Soil 192, 31-35. doi: 10.1023/A:1004265913770.
36. Schmohl, N., and Horst, W. J. (2000). Cell wall pectin content modulates aluminium sensitivity of Zea mays (L.) cells grown in suspension culture. Plant Cell Environ. 23, 735-742. doi: 10.1046/j.1365-3040.2000.00591.x.
37. Schmohl, N., Pilling, J., Fisahn, J., and Horst, W. J. (2000). Pectin methylesterase modulates aluminium sensitivity in Zea mays and Solanum tuberosum. Physiol. Plant. 109, 419-427. doi: 10.1034/j.1399-3054.2000.100408.x.
38. Shen, H., Yan, X., Zhao, M., Zheng, S., and Wang, X. (2002). Exudation of organic acids in common bean as related to mobilization of aluminum-and iron-bound phosphates. Environ. Exp. Bot. 48, 1-9. doi: 10.1016/S0098-8472(02)00009-6.
39. Shi, R. H., Xie, G. S., Zeng, H. L., and Zhang, D. P. (2007). Physiological mechanism of alleviating aluminum toxicity in rice seedling root by exogenous organic acids.Chinese J. Eco-Agriculture 4, 026.
40. Sivaguru, M., and Horst, W. J. (1998). The distal part of the transition zone is the most aluminum-sensitive apical root zone of maize 1. Plant Physiol. 116, 155-163. doi: 10.1104/pp.116.1.155.
41. Sivaguru, M., Horst, W. J., Eticha, D., and Matsumoto, H. (2006). Aluminum inhibits apoplastic flow of high-molecular weight solutes in root apices of Zea mays L. J. Plant Nutr. Soil Sci. 169, 679-690. doi: 10.1002/jpln.200620603.
42. Sivaguru, M., Volkmann, D., Felle, H. H., and Horst, W. J. (1999). Impacts of aluminum on the cytoskeleton of the maize root apex. short-term effects on the distal part of the transition zone. Plant Physiol. 119, 1073-1082. doi: 10.1104/pp.119.3.1073.
43. Stass, A., Smit, I., Eticha, D., Oettler, G., and Johannes Horst, W. (2008). The significance of organic-anion exudation for the aluminum resistance of primary triticale derived from wheat and rye parents differing in aluminum resistance. J. Plant Nutr. Soil Sci. 171, 634-642. doi: 10.1002/jpln.200700331.
44. Taylor, G. J., McDonald-Stephens, J. L., Hunter, D. B., Bertsch, P. M., Elmore, D., Rengel, Z., et al. (2000). Direct measurement of aluminum uptake and distribution in single cells of Chara corallina. Plant Physiol. 123, 987-996. doi: 10.1104/pp.123.3.987.
45. Verbelen, J.-P., De Cnodder, T., Le, J., Vissenberg, K., and Baluška, F. (2006). The root apex of Arabidopsis thaliana consists of four distinct zones of growth activities: meristematic zone, transition zone, fast elongation zone and growth terminating zone.Plant Signal. Behav. 1, 296-304. doi: 10.4161/psb.1.6.3511.
46. Wang, Y., Stass, A., and Horst, W. J. (2004). Apoplastic binding of aluminum is involved in silicon-induced amelioration of aluminum toxicity in maize. Plant Physiol. 136, 3762-3770. doi: 10.1104/pp.104.045005.
47. Yang, J. L., Zhu, X. F., Peng, Y. X., Zheng, C., Li, G. X., Liu, Y., et al. (2011a). Cell wall hemicellulose contributes significantly to aluminum adsorption and root growth inArabidopsis. Plant Physiol. 155, 1885-1892. doi: 10.1104/pp.111.172221.
48. Yang, J. L., Zhu, X. F., Zheng, C., Zhang, Y. J., and Zheng, S. J. (2011b). Genotypic differences in Al resistance and the role of cell-wall pectin in Al exclusion from the root apex in Fagopyrum tataricum. Ann. Bot. 107, 371-378. doi: 10.1093/aob/mcq254.
49. Yang, J., Li, Y., Zhang, Y., and Zhang, S. (2008). Cell wall polysaccharides are specifically involved in the exclusion of aluminum from the rice root apex. Plant Physiol. 146, 602-611. doi: 10.1104/pp.107.111989.
50. Yu, M., Ming Feng, Y., and Goldbach, H. E. (2006). Mist culture for mass harvesting of root border cells: aluminum effects. J. Plant Nutr. Soil Sci. 169, 670-674. doi: 10.1002/jpln.200620604.
51. Zhu, X. F., Lei, G. J., Wang, Z. W., Shi, Y. Z., Braam, J., Li, G. X., et al. (2013). Coordination between apoplastic and symplastic detoxification confers plant aluminum resistance. Plant Physiol. 162, 1947-1955. doi: 10.1104/pp.113.219147.