石灰土壤中植物铁营养生理生化的研究进展

doi:10.11924/j.issn.1000-6850.casb17110069

摘要/Abstract

摘要： 为了阐明石灰土中植物缺铁失绿的生理生化机理，综述了石灰土或重碳酸盐胁迫下植物对铁吸收和转运的研究进展。在石灰土壤中，由于存在CaCO3或MgCO3，它们与CO2和H2O反应形成过量的碳酸氢根离子（也叫重碳酸盐），从而导致了石灰土中富含重碳酸盐。总结了重碳酸盐改变土壤pH，降低了土壤中铁的可利用性，从而限制了植物对土壤中铁的吸收；另一方面，植物在重碳酸盐胁迫下，诱导植物根系产生一系列的生理生化反应响应低铁生境，包括植物根系分泌相关的物质或质子到根际土壤酸化土壤，诱导根系铁还原酶基因表达从而增强铁还原酶活性，以及诱导铁转运体基因的表达等。石灰土壤中的存在大量的重碳酸盐，针对该土壤环境的特殊性，未来应加强以下几个方面的研究，（1）重点研究重碳酸盐对铁在植物组织之间的长距离运输的影响，挖掘重碳盐影响铁转运的分子机制；（2）植物细胞内的铁蛋白是否受到重碳酸盐的影响，仍然需要开展相关的研究；（3）进一步研究土壤中的微生物与重碳酸盐在植物胁迫中的作用。

Abstract: The aim is to elucidate the physiological and biochemical mechanism that iron deficiency induced chlorotic symptom of plant in calcareous soil. We summarized that the bicarbonate changed soil pH value and then reduced the iron availability in soil, so that it limited the iron uptake in plants. Additionally, the bicarbonate stress induced a series of physiological and biochemical reactions in roots in response to the low iron habitat, including the roots secreting relative substances or proton to the rhizosphere soil to acidify soil, inducing the expression of ferric reductase gene and iron transporter gene to enhance iron reductase activity and iron uptake from soil. According to the characteristics of calcareous soil, the future research should be carried out on: (1) highlighting the effect of bicarbonate on iron transport from root to leaf to explain molecular mechanism of chlorotic symptom; (2) clarifying the effect of bicarbonate on the expression of ferritin gene in cell; (3) exploring the relationship between microorganisms and bicarbonate to reveal the characteristics of plant adaptation to calcareous soil.

刘伦衔＋,张习敏＋,苏志孟,乙引. 石灰土壤中植物铁营养生理生化的研究进展[J]. 中国农学通报, 2018, 34(11): 6-12.

参考文献

[1] Briat, J. F., Dubos, C. Gaymard, F. Iron nutrition, biomass production, and plant product quality[J]. Trends in Plant Science , 2015, 20, 33-40.
[2] Thomine, S. Vert, G. Iron transport in plants: better be safe than sorry. Current Opinion in Plant Biology[J]. 2013.16, 322-327
[3] Mengel, K., Kirkby, E. A., Kosegarten, H. Appel, T. Principles of Plant Nutrition. International Potash Institute[M], 1982.
[4] Chen, Y. Barak, P. Iron Nutrition of Plants in Calcareous Soils. Advances in Agronomy[J]. 1982. 35, 217-240.
[5] Murata, Y., Itoh, Y., Iwashita, T. Namba, K. Transgenic Petunia with the Iron(III)-Phytosiderophore Transporter Gene Acquires Tolerance to Iron Deficiency in Alkaline Environments[J]. Plos One. 2015.10(3), e0120227.
[6] Zuo, Y., Ren, L., Zhang, F. Jiang, R. Bicarbonate concentration as affected by soil water content controls iron nutrition of peanut plants in a calcareous soil[J]. Plant Physiology Biochemistry. 2007. 45, 357.
[7] 任丽轩. 石灰性土壤上HCO3^-诱导花生缺铁失绿机制[J]. 生态学报. 2005. 25, 795-801.
[8] Haleem, A. A., Loeppert, R. H. Anderson, W. B. Role of soil carbonate and iron oxide in iron nutrition of soybean in calcareous soils of Egypt and the United States[J]. 1995. 59, 307-314.
[9] De, B. B., Mclean, E., Andersson, M. Rogers, L. Iodine deficiency in 2007: global progress since 2003[J]. Food Nutrition Bulletin.2008. 29, 195.
[10] Yuan, D. X. WORLD CORRELATION OF KARST ECOSYSTEM: OBJECTIVES AND IMPLEMENTATION PLAN[J]. Advance in Earth Sciences. 2001. 16, 461-466.
[11] Carpena-Artes, O., Moreno, J. J., Lucena, J. J. Carpena-Ruiz, R. O. Response to iron chlorosis of different hydroponically grown Citrus varieties[J]. Springer Netherlands. 1995. 147-151.
[12] Lucena, J. J. Effects of bicarbonate, nitrate and other environmental factors on iron deficiency chlorisis[J]. A review. Journal of Plant Nutrition. 2000. 23, 1591-1606.
[13] 张福锁. 重碳酸盐抑制向日葵吸收利用铁的机理[J]. 土壤. 1992.293-296.
[14] Zheng, Y. C. Wang, S. J. Seological cause of calcareous soil erosion and land rocky desertification in karst area, Guizhou province [J]. Resources Enuironment in the Yangtza Basin. 2002. 11, 461-465.
[15] Hopkins, B. Ellsworth, J.
[16] Ao, T. Y., Chaney, R. L., Korcak, R. F., Fan, F. Faust, M. Influence of soil moisture level on apple iron chlorosis development in a calcareous soil[J]. Plant Soil . 1987. 104, 85-92.
[17] Zheng, Y. Effects of Soil Moisture and Bicarbonate on Iron Chlorosis of Peanut Grown on Calcareous Soil[J]. Review of China Agricultural Science Technology 2000.03.234-237
[18] Elgala, A. M. Maier, R. H. Chemical forms of plant and soil iron as influenced by soil moisture[J]. Plant Soil. 1964. 21, 201-212.
[19] Colombo, C., Palumbo, G., He, J. Z., Pinton, R. Cesco, S. Review on iron availability in soil: interaction of Fe minerals, plants, and microbes[J]. Journal of Soils Sediments. 2014. 14, 538-548.
[20] Krohling, C. A. et al. Ecophysiology of iron homeostasis in plants[J]. Soil Science Plant Nutrition. 2016. 62, 39-47
[21] Mengel, K. Iron availability in plant tissues-iron chlorosis on calcareous soils[J]. Plant Soil. 1994. 165, 275-283.
[22] Guerinot, M. L. Yi, Y. Iron: Nutritious, Noxious, and Not Readily Available[J]. Plant Physiology. 1994. 104, 815-820.
[23] Lindsay, Willard, L., Thorne D., W. Bicarbonate ion and oxygen level as related to chlorosis[J]. Soil Science. 1954. 77, 271-280.
[24] Boxma, R. Bicarbonate as the most important soil factor in lime-induced chlorosis in the netherlands[J]. Plant Soil. 1972. 37, 233-243.
[25] Mengel, K., Breininger, M. T. Bübl, W. Bicarbonate, the most important factor inducing iron chlorosis in vine grapes on calcareous soil[J]. Plant Soil. 1984. 81, 333-344.
[26] Boukhalfa, H. Crumbliss, A. L. Chemical aspects of siderophore mediated iron transport[J]. Biometals. 2002. 15, 325-339.
[27] Romheld, V. Marschner, H. Mobilization of iron in the rhizosphere of different plant species[J]. Advances in Plant Nutrition. 1986. 3, 178-182
[28] Liu, Y. et al. Assessing the contributions of lateral roots to element uptake in rice using an auxin-related lateral root mutant[J]. Plant Soil. 2013. 372, 125-136
[29] Lee, J. A. Woolhouse, H. W. A comparative study of bicarbonate inhibition of root growth of certain grasses[J]. New Phytologist. 1969. 68, 1-11.
[30] Gruber, B. Kosegarten, H. Depressed growth of non‐chlorotic vine grown in calcareous soil is an iron deficiency symptom prior to leaf chlorosis[J]. Journal of Plant Nutrition and Soil Science = Zeitschrift fuer Pflanzenernaehrung und Bodenkunde. 2015. 165, 111-117.
[31] Gruber, B. Kosegarten, H. Inhibited leaf growth of plants grown in alkaline solution and on calcareous soils is a more sensitive Fe-deficiency symptom than leaf chlorosis[J]. 2001.
[32] Yang, X., R?mheld, V. Marschner, H. Effect of bicarbonate on root growth and accumulation of organic acids in Zn-inefficient and Zn-efficient rice cultivars (Oryza sativa L.) [J]. Plant Soil 1994.164, 1-7.
[33] Li, Q., Yang, A. Zhang, W. H. Efficient acquisition of iron confers greater tolerance to saline-alkaline stress in rice (Oryza sativaL.) [J]. Journal of Experimental Botany. 2016. 67, 6431-6444.
[34] Covarrubias, J. I. Rombolà, A. D. Physiological and biochemical responses of the iron chlorosis tolerant grapevine rootstock 140 Ruggeri to iron deficiency and bicarbonate[J]. Plant Soil. 2013. 370, 305-315.
[35] Uren, N. C. Reisenauer, H. M. The role of root exudates in nutrient acquisition[J]. Advances in Plant Nutrition .1988. 3,203-207.
[36] Jones, D. L. Darrah, P. R. Role of root derived organic acids in the mobilization of nutrients from the rhizosphere[J]. Plant Soil. 1994. 166, 247-257.
[37] M'Sehli, W. et al. Root exudation and rhizosphere acidification by two lines of Medicago ciliaris in response to lime-induced iron deficiency[J]. Plant Soil. 2008.312, 151-162.
[38] Zhao, K. Wu, Y. Effect of Zn deficiency and excessive bicarbonate on the allocation and exudation of organic acids in two Moraceae plants[J]. Acta Geochimica. 2017. 1-9.
[39] Rodríguez-Celma, J. et al. Characterization of flavins in roots of Fe-deficient strategy I plants, with a focus on Medicago truncatula[J]. Plant Cell Physiology. 2011. 52, 2173-2189.
[40] Rose, M. T., Rose, T. J., Pariascatanaka, J., Widodo Wissuwa, M. Revisiting the role of organic acids in the bicarbonate tolerance of zinc-efficient rice genotypes[M]. 2011.
[41] Tato, L., De, N. P., Donnini, S. Zocchi, G. Low iron availability and phenolic metabolism in a wild plant species (Parietaria judaica L.) [J]. Plant Physiology Biochemistry Ppb. 2013. 72, 145.
[42] Yang, C., Guo, W. Shi, D. Physiological Roles of Organic Acids in Alkali-Tolerance of the Alkali-Tolerant Halophyte Chloris virgate[J]. Agronomy Journal. 2010.102.
[43] Guo, S. H., Niu, Y. J., Zhai, H., Han, N. Du, Y. P. Effects of alkaline stress on organic acid metabolism in roots of grape hybrid rootstocks[J]. Scientia Horticulturae. 2018. 227, 255-260 .
[44] Yang, G. H. Alkali stress induced the accumulation and secretion of organic acids in wheat[J]. African Journal of Agricultural Research. 2012. 18,7.
[45] Donnini, S., Castagna, A., Ranieri, A. Zocchi, G. Differential responses in pear and quince genotypes induced by Fe deficiency and bicarbonate[J]. Journal of Plant Physiology. 2009. 166, 1181-1193.
[46] Qian, Z., Zhang, Q., Zhang, X., Han, Z. Wang, Y. Cloning and characterization of MxHA7 , a plasma membrane H + -ATPase gene related to high tolerance of Malus xiaojinensis to iron deficiency[J]. Acta Physiologiae Plantarum. 2014. 36, 955-962.
[47] Lucena, C. et al. Bicarbonate blocks the expression of several genes involved in the physiological responses to Fe deficiency of Strategy I plants[J]. Functional Plant Biology. 2007. 34, 1002-1009.
[48] Martínezcuenca, M. R., Legaz, F., Fornerginer, M. á., Primomillo, E. Iglesias, D. J. Bicarbonate blocks iron translocation from cotyledons inducing iron stress responses in Citrus roots[J]. Journal of Plant Physiology. 2013. 170, 899-905.
[49] Martínez-Cuenca, M. R., Iglesias, D. J., Forner-Giner, M. A., Primo-Millo, E. Legaz, F. The effect of sodium bicarbonate on plant performance and iron acquisition system of FA-5 (Forner-Alcaide 5) citrus seedlings[J]. Acta Physiologiae Plantarum. 2013.35, 2833-2845.
[50] Rayadíaz, S., Sánchezrodríguez, A. R., Segurafernández, J. M., Del, M. C. Quesadamoraga, E. Entomopathogenic fungi-based mechanisms for improved Fe nutrition in sorghum plants grown on calcareous substrates[J]. Plos One. 2017. 12, e0185903.
[51] Brown, J. C. Tiffin, L. O. Obligatory Reduction of Ferric Chelates in Iron Uptake by Soybeans[J]. Plant Physiology. 1972. 50, 208
[52] Robinson, N. J., Procter, C. M., Connolly, E. L. Guerinot, M. L. A ferric-chelate reductase for iron uptake from soils[J]. Nature. 1999 397, 694-697.
[53] Li, L., Cheng, X. Ling, H. Q. Isolation and characterization of Fe(III)-chelate reductase gene LeFRO1 in tomato[J]. Plant Molecular Biology. 2004.5 4, 125-136
[54] Waters, B. M., Blevins, D. G. Eide, D. J. Characterization of FRO1, a pea ferric-chelate reductase involved in root iron acquisition[J]. Plant Physiology. 2002. 129, 85.
[55] Waters, B. M. et al. Ethylene involvement in the regulation of the H + -ATPase CsHA1 gene and of the new isolated ferric reductase CsFRO1 and iron transporter CsIRT1 genes in cucumber plants[J]. Plant Physiology Biochemistry 2007.45, 293-301.
[56] Garc铆A, M. J. et al. Hypoxia and bicarbonate could limit the expression of iron acquisition genes in Strategy I plants by affecting ethylene synthesis and signaling in different ways[J]. Physiologia Plantarum. 2014. 150, 95.
[57] En-Jung, H. Waters, B. M. Alkaline stress and iron deficiency regulate iron uptake and riboflavin synthesis gene expression differently in root and leaf tissue: implications for iron deficiency chlorosis[J]. Journal of Experimental Botany. 2016. 67, 5671-5685.
[58] 崔骁勇, 曹一平张福锁. 氮素形态及HCO-3对豌豆铁素营养的影响[J]. 植物营养与肥料学报. 2000. 6, 84-90.
[59] R?mheld, V. Marschner, H. Mechanism of Iron Uptake by Peanut Plants 1[J]. Plant Physiology. 1983.
[60] Eide, D., Broderius, M., Fett, J. Guerinot, M. L. A novel iron-regulated metal transporter from plants identified by functional expression in yeast[J]. Proceedings of the National Academy of Sciences of the United States of America. 1996. 93, 5624-5628.
[61] Eckhardt, U., Mas, M. A. Buckhout, T. J. Two iron-regulated cation transporters from tomato complement metal uptake-deficient yeast mutants[J]. Plant Molecular Biology. 2001. 45, 437-448.
[62] Cohen, C. K., Fox, T. C., Garvin, D. F. Kochian, L. V. The role of iron-deficiency stress responses in stimulating heavy-metal transport in plants[J]. Plant Physiology. 1998. 116, 1063.
[63] Bughio, N., Yamaguchi, H., Nishizawa, N. K., Nakanishi, H. Mori, S. Cloning an iron‐regulated metal transporter from rice[J]. Journal of Experimental Botany. 2002. 53, 1677.
[64] G, V. et al. IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth[J]. Plant Cell. 2002. 14, 1223-1233.
[65] Wang, H. Y. et al. Iron deficiency-mediated stress regulation of four subgroup Ib BHLH genes in Arabidopsis thaliana[J]. Planta . 2007. 226, 897.
[66] Yuan, Y. et al. FIT interacts with AtbHLH38 and AtbHLH39 in regulating iron uptake gene expression for iron homeostasis in Arabidopsis. Cell research. 2008. 18, 385.
[67] Vannozzi, A. et al. Transcriptional Characterization of a Widely-Used Grapevine Rootstock Genotype under Different Iron-Limited Conditions[J]. Frontiers in Plant Science. 2016.7, 1994.
[68] Hell, R. Stephan, U. W. Iron uptake, trafficking and homeostasis in plants[J]. Planta. 2003. 216, 541-551.
[69] Durrett, T. P., Gassmann, W. Rogers, E. E. The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation[J]. Plant Physiology. 2007. 144, 197-205.
[70] Yokosho, K. Ma, J. F. OsFRDL1 Is a Citrate Transporter Required for Efficient Translocation of Iron in Rice[J]. Plant Physiology. 2009. 149, 297-305.
[71] Takanashi, K. et al. LjMATE1: a citrate transporter responsible for iron supply to the nodule infection zone of Lotus japonicus[J]. Plant Cell Physiology. 2013. 54, 585-594.
[72] Hannetz, R. et al. New insights into Fe localization in plant tissues[J]. Frontiers in Plant Science. 2013. 4, 350.
[73] Kruger, C., Berkowitz, O., Stephan, U. W. Hell, R. A metal-binding member of the late embryogenesis abundant protein family transports iron in the phloem of Ricinus communis L[J]. Journal of Biological Chemistry. 2002. 277, 25062-25069.
[74] Waters, B. M. et al. Mutations in Arabidopsis Yellow Stripe-Like1 and Yellow Stripe-Like3 Reveal Their Roles in Metal Ion Homeostasis and Loading of Metal Ions in Seeds[J]. Plant Physiology. 2006. 141, 1446.
[75] Divol, F. et al. The Arabidopsis YELLOW STRIPE LIKE4 and 6 Transporters Control Iron Release from the Chloroplast[J]. Plant Cell. 2013. 25, 1040.
[76] Petit, J. M., Briat, J. F. Lobréaux, S. Structure and differential expression of the four members of the Arabidopsis thaliana ferritin gene family[J]. Biochemical Journal. 2001. 359, 575.