This review provides an examination of the marsh spot disease in beans and the roles played by its causal factor, manganese (Mn) deficiency. The discovery of the marsh spot disease, its relation with Mn deficiency, and how it can be treated are discussed. Mn serves as a cofactor and a catalyst in various metabolic processes in different cell compartments, such as the oxygen-evolving complex of photosystem II (PSII) or reactive oxygen species scavenging. Some major quantitative trait loci (QTL) and putative candidate genes associated with Mn content in plants, especially in plant seeds, have been identified. Marsh spot disease in cranberry common bean is controlled by several major genes with significant additive and epistatic effects. They provide valuable clues for QTL candidate gene prediction and an improved understanding of the genetic mechanisms responsible for marsh spot resistance in plants.
References
[1]
Henkens, C.H. (1958) The Prevention of Marsh Spot in Peas by Spraying with Manganese Sulphate. Landbouwvoorlichting, 15, 262-265.
[2]
Reynolds, J.D. (1955) Marsh Spot of Peas: A Review of Present Knowledge. Journal of the Science of Food and Agriculture, 6, 725-734. https://doi.org/10.1002/jsfa.2740061201
[3]
Piper, C.S. (1941) Marsh Spot of Peas: A Manganese Deficiency Disease. The Journal of Agricultural Science, 31, 448-453. https://doi.org/10.1017/S0021859600049637
[4]
Heintze, S.G. (1938) Readily Soluble Manganese of Soils and Marsh Spot of Peas. The Journal of Agricultural Science, 28, 175-186. https://doi.org/10.1017/S0021859600050590
[5]
Lacey, M.S. (1934) Studies in Bacteriosis: Xxi. An Investigation of Marsh Spot of Peas: With a Note on the Morphological Structure. Annals of Applied Biology, 21, 621-640. https://doi.org/10.1111/j.1744-7348.1934.tb07465.x
[6]
Biddle, A.J. and Cattlin, N.D. (2007) Pests, Diseases, and Disorders of Peas and Beans: A Colour Handbook. CRC Press, London. https://doi.org/10.1201/b15137
[7]
Howard, R.J., Garland, J.A. and Seaman, W.L. (1994) Diseases and Pests of Vegetable Crops in Canada. Canadian Phytopathological Society, Ottawa.
De Bruyn, H.L.G. (1933) Kwade Harten van de Erwten. Tijdschrift Over Plantenziekten, 39, 281-318. https://doi.org/10.1007/BF02807372
[10]
Maillard, A., Diquelou, S., Billard, V., Laine, P., Garnica, M., Prudent, M., Garcia-Mina, J.M., Yvin, J.C. and Ourry, A. (2015) Leaf Mineral Nutrient Remobilization during Leaf Senescence and Modulation by Nutrient Deficiency. Frontiers in Plant Science, 6, Article No. 317. https://doi.org/10.3389/fpls.2015.00317
[11]
Graham, R.D., Hannam, R.J. and Uren, N.C. (1988) Manganese in Soils and Plants. Vol. 33, Springer, Dordrecht. https://doi.org/10.1007/978-94-009-2817-6
[12]
Furneaux, B.S. and Glasscock, H.H. (1936) Soils in Relation to Marsh Spot of Pea Seed. The Journal of Agricultural Science, 26, 59-84. https://doi.org/10.1017/S0021859600021808
[13]
De Bruyn, H.L.G. (1939) Mn-Deficiency as the Cause of Marsh Spot of Pea Seeds. Tijdschrift Over Plantenziekten, 45, 106-120. https://doi.org/10.1007/BF02651193
[14]
Jia, B., Conner, R.L., Khan, N., Hou, A., Xia, X. and You, F.M. (2021) Inheritance of Marsh Spot Disease Resistance in Cranberry Common Bean (Phaseolus vulgaris L.). The Crop Journal. (In Press) https://doi.org/10.1016/j.cj.2021.05.013
[15]
Pethybridge, G.H. (1936) Marsh Spot in Pea Seeds: Is It a Deficiency Disease. Journal of the Ministry of Agriculture, 43, 55-58.
[16]
Samuel, G. and Piper, C.S. (1929) Manganese as an Essential Element for Plant Growth. Annals of Applied Biology, 16, 493-524. https://doi.org/10.1111/j.1744-7348.1929.tb07630.x
[17]
Moraghan, J. and Grafton, G. (2000) ‘Marsh Spot’ in Cranberry Bean Seed. Annual Report of the Bean Improvement Cooperative, 43, 9-10.
[18]
Koopman, C. (1937) Invloed van mangaansulfaatbespuiting tegen kwaadhartigheid bij schokkererwten. Tijdschr Over Plantenziekten, 43, 64-66. https://doi.org/10.1007/BF01988574
[19]
Lewis, A.H. (1939) Manganese Deficiencies in Crops. I. Spraying Pea Crops with Solutions of Manganese Salts to Eliminate Marsh-Spot. Empire Journal of Experimental Agriculture, 7, 150-154.
[20]
Hoecker, N., Leister, D. and Schneider, A. (2017) Plants Contain Small Families of UPF0016 Proteins Including the PHOTOSYNTHESIS AFFECTED MUTANT71 Transporter. Plant Signaling & Behavior, 12, Article No. e1278101. https://doi.org/10.1080/15592324.2016.1278101
[21]
Dasgupta, J., Ananyev, G.M. and Dismukes, G.C. (2008) Photoassembly of the Water-Oxidizing Complex in Photosystem II. Coordination Chemistry Reviews, 252, 347-360. https://doi.org/10.1016/j.ccr.2007.08.022
[22]
Foyer, C.H. and Noctor, G. (2003) Redox Sensing and Signalling Associated with Reactive Oxygen in Chloroplasts, Peroxisomes and Mitochondria. Physiologia Plantarum, 119, 355-364. https://doi.org/10.1034/j.1399-3054.2003.00223.x
[23]
Gutteridge, J.M.C. and Halliwell, B. (2010) Antioxidants: Molecules, Medicines, and Myths. Biochemical and Biophysical Research Communications, 393, 561-564. https://doi.org/10.1016/j.bbrc.2010.02.071
[24]
Schmidt, S.B., Jensen, P.E. and Husted, S. (2016) Manganese Deficiency in Plants: The Impact on Photosystem II. Trends in Plant Science, 21, 622-632. https://doi.org/10.1016/j.tplants.2016.03.001
[25]
Broadley, M., Brown, P., Cakmak, I., Rengel, Z. and Zhao, F.-J. (2012) Function of Nutrients. In: Marschner, H., Ed., Marschner’s Mineral Nutrition of Higher Plants, Academic Press, Oxford, 191-248. https://doi.org/10.1016/B978-0-12-384905-2.00007-8
[26]
Engelsma, G. (1972) A Possible Role of Divalent Manganese Ions in the Photoinduction of Phenylalanine Ammonia-Lyase. Plant Physiology, 50, 599-602. https://doi.org/10.1104/pp.50.5.599
[27]
Hebbern, C.A., Laursen, K.H., Ladegaard, A.H., Schmidt, S.B., Pedas, P., Bruhn, D., Schjoerring, J.K., Wulfsohn, D. and Husted, S. (2009) Latent Manganese Deficiency Increases Transpiration in Barley (Hordeum vulgare). Plant Physiology, 135, 307-316. https://doi.org/10.1111/j.1399-3054.2008.01188.x
[28]
Rohdich, F., Lauw, S., Kaiser, J., Feicht, R., Köhler, P., Bacher, A. and Eisenreich, W. (2006) Isoprenoid Biosynthesis in Plants 2C-methyl-d-erythritol-4-phosphate Synthase (IspC Protein) of Arabidopsis thaliana. The FEBS Journal, 273, 4446-4458. https://doi.org/10.1111/j.1742-4658.2006.05446.x
[29]
Ohki, K., Boswell, F.C., Parker, M.B., Shuman, L.M. and Wilson, D.O. (1979) Critical Manganese Deficiency Level of Soybean Related to Leaf Position. Agronomy Journal, 71, 233-234. https://doi.org/10.2134/agronj1979.00021962007100020004x
[30]
Shenker, M., Plessner, O.E. and Tel-Or, E. (2004) Manganese Nutrition Effects on Tomato Growth, Chlorophyll Concentration, and Superoxide Dismutase Activity. Journal of Plant Physiology, 161, 197-202. https://doi.org/10.1078/0176-1617-00931
[31]
Chu, H.-H., Car, S., Socha, A.L., Hindt, M.N., Punshon, T. and Guerinot, M.L. (2017) The Arabidopsis MTP8 Transporter Determines the Localization of Manganese and Iron in Seeds. Scientific Reports, 7, Article No. 11024. https://doi.org/10.1038/s41598-017-11250-9
[32]
Giles, C.D., Brown, L.K., Adu, M.O., Mezeli, M.M., Sandral, G.A., Simpson, R.J., Wendler, R., Shand, C.A., Menezes-Blackburn, D., Darch, T., Stutter, M.I., Lumsdon, D.G., Zhang, H., Blackwell, M.S., Wearing, C., Cooper, P., Haygarth, P.M. and George, T.S. (2017) Response-Based Selection of Barley Cultivars and Legume Species for Complementarity: Root Morphology and Exudation in Relation to Nutrient Source. Plant Science, 255, 12-28. https://doi.org/10.1016/j.plantsci.2016.11.002
[33]
Guerinot, M.L. (2000) The ZIP Family of Metal Transporters. Biochimica et Biophysica Acta (BBA)-Biomembranes, 1465, 190-198. https://doi.org/10.1016/S0005-2736(00)00138-3
[34]
Kolaj-Robin, O., Russell, D., Hayes, K.A., Pembroke, J.T. and Soulimane, T. (2015) Cation Diffusion Facilitator Family: Structure and Function. FEBS Letters, 589, 1283-1295. https://doi.org/10.1016/j.febslet.2015.04.007
[35]
Renfrew, A.K., O’Neill, E.S., Hambley, T.W. and New, E.J. (2018) Harnessing the Properties of Cobalt Coordination Complexes for Biological Application. Coordination Chemistry Reviews, 375, 221-233. https://doi.org/10.1016/j.ccr.2017.11.027
[36]
Montanini, B., Blaudez, D., Jeandroz, S., Sanders, D. and Chalot, M. (2007) Phylogenetic and Functional Analysis of the Cation Diffusion Facilitator (CDF) Family: Improved Signature and Prediction of Substrate Specificity. BMC Genomics, 8, Article No. 107. https://doi.org/10.1186/1471-2164-8-107
[37]
Pittman, J.K. and Hirschi, K.D. (2016) Phylogenetic Analysis and Protein Structure Modelling Identifies Distinct Ca2+/Cation Antiporters and Conservation of Gene Family Structure within Arabidopsis and Rice Species. Rice, 9, Article No. 3. https://doi.org/10.1186/s12284-016-0075-8
[38]
Cao, J. (2019) Molecular Evolution of the Vacuolar Iron Transporter (VIT) Family Genes in 14 Plant Species. Genes, 10, Article No. 144. https://doi.org/10.3390/genes10020144
[39]
Edmond, C., Shigaki, T., Ewert, S., Nelson, M.D., Connorton, J.M., Chalova, V., Noordally, Z. and Pittman, J.K. (2009) Comparative Analysis of CAX2-Like Cation Transporters Indicates Functional and Regulatory Diversity. Biochemical Journal, 418, 145-154. https://doi.org/10.1042/BJ20081814
[40]
Kamiya, T., Akahori, T., Ashikari, M. and Maeshima, M. (2006) Expression of the Vacuolar Ca2+/H+ Exchanger, OSCAX1a, in Rice: Cell and Age Specificity of Expression, and Enhancement by Ca2+. Plant and Cell Physiology, 47, 96-106. https://doi.org/10.1093/pcp/pci227
[41]
Eroglu, S., Meier, B., von Wirén, N. and Peiter, E. (2016) The Vacuolar Manganese Transporter mtp8 Determines Tolerance to Iron Deficiency-Induced Chlorosis in Arabidopsis. Plant Physiology, 170, 1030-1045. https://doi.org/10.1104/pp.15.01194
[42]
Thomine, S., Wang, R., Ward, J.M., Crawford, N.M. and Schroeder, J.I. (2000) Cadmium and Iron Transport by Members of a Plant Metal Transporter Family in Arabidopsis with Homology to Nramp Genes. Proceedings of the National Academy of Sciences of the United States of America, 97, 4991-4996. https://doi.org/10.1073/pnas.97.9.4991
[43]
Lanquar, V., Ramos, M.S., Lelièvre, F., Barbier-Brygoo, H., Krieger-Liszkay, A., Krämer, U. and Thomine, S. (2010) Export of Vacuolar Manganese by AtNRAMP3 and AtNRAMP4 Is Required for Optimal Photosynthesis and Growth under Manganese Deficiency. Plant Physiology, 152, 1986-1999. https://doi.org/10.1104/pp.109.150946
[44]
Koike, S., Inoue, H., Mizuno, D., Takahashi, M., Nakanishi, H., Mori, S. and Nishizawa, N.K. (2004) OsYSL2 Is a Rice Metal-Nicotianamine Transporter That Is Regulated by Iron and Expressed in the Phloem. The Plant Journal, 39, 415-424. https://doi.org/10.1111/j.1365-313X.2004.02146.x
[45]
Pedas, P., Ytting, C.K., Fuglsang, A.T., Jahn, T.P., Schjoerring, J.K. and Husted, S. (2008) Manganese Efficiency in Barley: Identification and Characterization of the Metal Ion Transporter HvIRT1. Plant Physiology, 148, 455-466. https://doi.org/10.1104/pp.108.118851
[46]
Marschner, H. (1995) Mineral Nutrition of Higher Plants. 2nd Edition, Academic Press, London, 233-234.
[47]
Eugene, V.M., David, P.M. and Benjamin, J.M. (1968) Manganese Absorption by Excised Barley Roots. Plant Physiology, 43, 527-530. https://doi.org/10.1104/pp.43.4.527
[48]
Humphries, J., Stangoulis, J. and Graham, R. (2007) Manganese. In: Barker, A.V. and Pilbeam, D.J., Eds., Handbook of Plant Nutrition, Taylor and Francis, Boca Raton, 351-366. https://www.worldcat.org/title/handbook-of-plant-nutrition/oclc/65205150
[49]
Waters, B.M. and Sankaran, R.P. (2011) Moving Micronutrients from the Soil to the Seeds: Genes and Physiological Processes from a Biofortification Perspective. Plant Science, 180, 562-574. https://doi.org/10.1016/j.plantsci.2010.12.003
[50]
Sasaki, A., Yamaji, N., Yokosho, K. and Ma, J.F. (2012) Nramp5 Is a Major Transporter Responsible for Manganese and Cadmium Uptake in Rice. Plant Cell, 24, 2155-2167. https://doi.org/10.1105/tpc.112.096925
[51]
Curie, C., Alonso, J.M., Le Jean, M., Ecker, J.R. and Briat, J.F. (2000) Involvement of NRAMP1 from Arabidopsis thaliana in Iron Transport. Biochemical Journal, 347, 749-755. https://doi.org/10.1042/bj3470749
[52]
Shao, J.F., Yamaji, N., Shen, R.F. and Ma, J.F. (2017) The Key to Mn Homeostasis in Plants: Regulation of Mn Transporters. Trends in Plant Science, 22, 215-224. https://doi.org/10.1016/j.tplants.2016.12.005
[53]
Cailliatte, R., Schikora, A., Briat, J.-F., Mari, S. and Curie, C. (2010) High-Affinity Manganese Uptake by the Metal Transporter Nramp1 Is Essential for Arabidopsis Growth in Low Manganese Conditions. Plant Cell, 22, 904-917. https://doi.org/10.1105/tpc.109.073023
[54]
Wu, D., Yamaji, N., Yamane, M., Kashino-Fujii, M., Sato, K. and Feng Ma, J. (2016) The HvNramp5 Transporter Mediates Uptake of Cadmium and Manganese, but Not Iron. Plant Physiology, 172, 1899-1910. https://doi.org/10.1104/pp.16.01189
[55]
Rieuwerts, J.S., Thornton, I., Farago, M.E. and Ashmore, M.R. (1998) Factors Influencing Metal Bioavailability in Soils: Preliminary Investigations for the Development of a critical loads approach for metals. Chemical Speciation & Bioavailability, 10, 61-75. https://doi.org/10.3184/095422998782775835
[56]
Yamaji, N., Sasaki, A., Xia, J.X., Yokosho, K. and Ma, J.F. (2013) A Node-Based Switch for Preferential Distribution of Manganese in Rice. Nature Communications, 4, Article No. 2442. https://doi.org/10.1038/ncomms3442
[57]
Ueno, D., Sasaki, A., Yamaji, N., Miyaji, T., Fujii, Y., Takemoto, Y., Moriyama, S., Che, J., Moriyama, Y., Iwasaki, K. and Ma, J.F. (2015) A Polarly Localized Transporter for Efficient Manganese Uptake in Rice. Nature Plants, 1, Article No. 15170. https://doi.org/10.1038/nplants.2015.170
[58]
Waters, B.M., Chu, H.-H., DiDonato, R.J., Roberts, L.A., Eisley, R.B., Lahner, B., Salt, D.E. and Walker, E.L. (2006) Mutations in Arabidopsis Yellow Stripe-Like1 and Yellow Stripe-Like3 Reveal Their Roles in Metal Ion Homeostasis and Loading of Metal Ions in Seeds. Plant Physiology, 141, 1446-1458. https://doi.org/10.1104/pp.106.082586
[59]
Milner, M.J., Seamon, J., Craft, E. and Kochian, L.V. (2013) Transport Properties of Members of the ZIP Family in Plants and Their Role in Zn and Mn Homeostasis. Journal of Experimental Botany, 64, 369-381. https://doi.org/10.1093/jxb/ers315
[60]
Zhang, Y., Xu, Y.-H., Yi, H.-Y. and Gong, J.-M. (2012) Vacuolar Membrane Transporters OsVIT1 and OsVIT2 Modulate Iron Translocation between Flag Leaves and Seeds in Rice. The Plant Journal, 72, 400-410. https://doi.org/10.1111/j.1365-313X.2012.05088.x
[61]
Connorton, J.M., Jones, E.R., Rodríguez-Ramiro, I., Fairweather-Tait, S., Uauy, C. and Balk, J. (2017) Wheat Vacuolar Iron Transporter TaVIT2 Transports Fe and Mn and Is Effective for Biofortification. Plant Physiology, 174, 2434-2444. https://doi.org/10.1104/pp.17.00672
[62]
Enrico, M., Stefan, M., Alexis, D.A. and Réka, N. (2012) Vacuolar Transporters in Their Physiological Context. Annual Review of Plant Biology, 63, 183-213. https://doi.org/10.1146/annurev-arplant-042811-105608
[63]
Thomine, S., Lelièvre, F., Debarbieux, E., Schroeder, J.I. and Barbier-Brygoo, H. (2003) AtNRAMP3, a Multispecific Vacuolar Metal Transporter Involved in Plant Responses to Iron Deficiency. The Plant Journal, 34, 685-695. https://doi.org/10.1046/j.1365-313X.2003.01760.x
[64]
Lanquar, V., Lelièvre, F., Bolte, S., Hamès, C., Alcon, C., Neumann, D., Vansuyt, G., Curie, C., Schröder, A., Krämer, U., Barbier-Brygoo, H. and Thomine, S. (2005) Mobilization of Vacuolar Iron by AtNRAMP3 and AtNRAMP4 Is Essential for Seed Germination on Low Iron. The EMBO Journal, 24, 4041-4051. https://doi.org/10.1038/sj.emboj.7600864
[65]
Mills, R.F., Doherty, M.L., López-Marqués, R.L., Weimar, T., Dupree, P., Palmgren, M.G., Pittman, J.K. and Williams, L.E. (2008) ECA3, a Golgi-Localized P2A-Type ATPase, Plays a Crucial Role in Manganese Nutrition in Arabidopsis. Plant Physiology, 146, 116-128. https://doi.org/10.1104/pp.107.110817
[66]
Delhaize, E., Gruber, B.D., Pittman, J.K., White, R.G., Leung, H., Miao, Y., Jiang, L., Ryan, P.R. and Richardson, A.E. (2007) A Role for the AtMTP11 Gene of Arabidopsis in Manganese Transport and Tolerance. The Plant Journal, 51, 198-210. https://doi.org/10.1111/j.1365-313X.2007.03138.x
[67]
Blair, M.W., Wu, X., Bhandari, D. and Astudillo, C. (2016) Genetic Dissection of ICP-Detected Nutrient Accumulation in the Whole Seed of Common Bean (Phaseolus vulgaris L.). Frontiers in Plant Science, 7, Article No. 219. https://doi.org/10.3389/fpls.2016.00219
[68]
Leplat, F., Pedas, P.R., Rasmussen, S.K. and Husted, S. (2016) Identification of Manganese Efficiency Candidate Genes in Winter Barley (Hordeum vulgare) Using Genome Wide Association Mapping. BMC Genomics, 17, Article No. 775. https://doi.org/10.1186/s12864-016-3165-5
[69]
Ates, D., Aldemir, S., Yagmur, B., Kahraman, A., Ozkan, H., Vandenberg, A. and Tanyolac, M.B. (2018) QTL Mapping of Genome Regions Controlling Manganese Uptake in Lentil Seed. G3: Genes|Genomes|Genetics, 8, 1409-1416. https://doi.org/10.1534/g3.118.200259
[70]
Ding, G., Yang, M., Hu, Y., Liao, Y., Shi, L., Xu, F. and Meng, J. (2010) Quantitative Trait loci Affecting Seed Mineral Concentrations in Brassica napus Grown with Contrasting Phosphorus Supplies. Annals of Botany, 105, 1221-1234. https://doi.org/10.1093/aob/mcq050
[71]
Klein, M.A. and Grusak, M.A. (2009) Identification of Nutrient and Physical Seed Trait QTL in the Model Legume Lotus japonicus. Genome, 52, 677-691. https://doi.org/10.1139/G09-039
[72]
Liu, C., Chen, G., Li, Y., Peng, Y., Zhang, A., Hong, K., Jiang, H., Ruan, B., Zhang, B., Yang, S., Gao, Z. and Qian, Q. (2017) Characterization of a Major QTL for Manganese Accumulation in Rice Grain. Scientific Reports, 7, Article No. 17704. https://doi.org/10.1038/s41598-017-18090-7
[73]
Nawaz, Z., Kakar, K.U., Li, X.-B., Li, S., Zhang, B., Shou, H.-X. and Shu, Q.-Y. (2015) Genome-Wide Association Mapping of Quantitative Trait Loci (QTLs) for Contents of Eight Elements in Brown Rice (Oryza sativa L.). Journal of Agricultural and Food Chemistry, 63, 8008-8016. https://doi.org/10.1021/acs.jafc.5b01191
[74]
Wu, J., Yuan, Y.-X., Zhang, X.-W., Zhao, J., Song, X., Li, Y., Li, X., Sun, R., Koornneef, M., Aarts, M.G.M. and Wang, X.-W. (2008) Mapping QTLs for Mineral Accumulation and Shoot Dry Biomass under Different Zn Nutritional Conditions in Chinese Cabbage (Brassica rapa L. ssp. Pekinensis). Plant and Soil, 310, 25-40. https://doi.org/10.1007/s11104-008-9625-1
