Plant Ionomics: Biological Language of Ions

Year 2023, Volume: 37 Issue: 1, 263 - 288, 01.06.2023

Berna Baş

https://doi.org/10.20479/bursauludagziraat.1133666

Abstract

Ionomics is a novel increasingly expanding multidisciplinary field and works quantification, mapping
of nutritional elements biography of living organisms and simultaneuos inter-elemental interaction into elements network system in response to external stimulants which are caused to eventually changes of physiology, development and gene expression. In this perspective, ionomic vision is comrehensive functional analysis of elements and also enables strategy development to control nutritional ion homeostasis in effect of metabolism, development, genome and ambient of organism. With this approach, elemental/ionic position of nutrient compounds in plants gives information about such as their adaptation to local and natural medium, disease status, disease resistant properties. This review is addressed introduction of ionomics, potential range of ionomic insights and their application areas, particularly roles in pathogenesis to disclose.

Keywords

Plant ionome, elemental analysis, nutrient elements, disease ionomy

Bitki İyonomiks: İyonların Biyolojik Dili

Abstract

İyonomiks giderek genişleyen, disiplinlerarası yeni bir alandır ve bir dış uyarana tepki sonucunda canlıların fizyolojisi, gelişimi ve gen ifadesinde değişimine neden olan besin elementlerinin niceliği, haritalanması ve aynı zamanda elementler ağ sisteminde elementler-arası etkileşimi çalışır. Bu perspektiften, iyonomun vizyonu elementlerin kapsamlı fonksiyonel analizidir ve organizmaların metabolizması, gelişimi, genomu ve çevresinin etkisiyle iyon dengesini kontrol etmek amacıyla stratejiler gelişimine de imkan vermektedir. Bu yaklaşımla bitkilerdeki besin maddelerinin elemental/iyonik pozisyonları bitkilerin doğal çevrelerine adaptasyonları, hastalık durumları ve hastalıklara dayanıklılık özellikleriyle ilgili bilgiler verir. Sunulan derleme iyonomiks konusunun tanıtımı, iyonomun potansiyeli ve uygulama alanları özellikle patogenezdeki rollerini ortaya koymak amacıyla ele alınmıştır.

Keywords

Bitki iyonomu, element analizi, besin elementleri, hastalık iyonomisi

References

• Acosta-Gamboa, L., Liu, M., Langley, S., Campbell, E., Castro-Guerrero, Z., Mendoza-Cozatl, N. and Lorence, A. 017. Moderate to severe water limitation differentially affects the phenome and ionome of Arabidopsis. Functional Plant Biology, 44: 94-106.
• Ajeesh Krishna, T.P., Maharajan, T., Victor Roch, G., Ignacimuthu, S. and Antony Ceasar, S. 2020. Structure, Function, Regulation and Phylogenetic Relationship of ZIP Family Transporters of Plants. Frontier of Plant Science, 11: 662.
• Amtmann, A., Troufflard, S. and Armengaud, P. 2008. The effect of potassium nutrition on pest and disease resistance in plants. Plant Physiologiy, 133: 682-691.
• Arslan, D. ve Özcan, M.M. 2011. Güney Anadolu’dan farklı çeşitlere ait zeytin yağlarının mineral madde içeriği üzerine lokasyon ve hasat döneminin etkisi. Uludağ Üniversitesi Ziraat Fakültesi Dergisi, 25(1): 11-26.
• Assunção, A., Cakmak, I., Clemens, S., González-Guerrero, M., Nawrocki, A. and Thomine, S. 2022. Micronutrient homeostasis in plants for more sustainable agriculture and healthier human nutrition. Journal of Experimental Botany, 73(6): 1789-1799.
• Astolfi, S. and Zuchi, S. 2013. Adequate S supply protects barley plants from adverse effects of salinity stress by increasing thiol contents. Acta Physiologiae Plantarum, 35: 175-181.
• Aznar, A., Chen, N.W.G., Thomine, S. and Dellagi, A. 2015. Immunity to plant pathogens and iron homeostasis. Plant Science, 240: 90-97.
• Bascom, C.S., Hepler, P.K. and Bezanilla, M. 2018. Interplay between ions, the cytoskeleton, and cell wall properties during tip growth. Plant Physiology, 176(1): 28-40.
• Baxter, I. 2010. Ionomics: The functional genomics of elements. Briefings in functional genomics, 9(2): 149- 156.
• Baxter, I., Brazelton, J.N., Yu, D., Huang, Y.S., Lahner, B., Yakubova, E., Li, Y., Bergelson, J., Borevitz, J.O., Nordborg, M., Vitek, O. and Salt, D.E. 2010. A coastal cline in sodium accumulation in Arabidopsis thaliana is driven by natural variation of the sodium transporter AtHKT1; 1. PLoS Genetics, 6(11): e1001193.
• Baxter, I. and Dilkes, B.P. 2012. Elemental profiles reflect plant adaptations to the environment. Science, 336(6089): 1661-1663.
• Bentsink, L., Yuan, K., Koornneef, M. and Vreugdenhil, D. 2003. The genetics of phytate and phosphate accumulation in seeds and leaves of Arabidopsis thaliana, using natural variation. Theoritical and Applied Genetics, 106: 1234-1243.
• Billard, V., Ourry, A., Maillard, A., Garnica, M., Coquet, L., Jouenne, T., Cruz, F., Garcia-Mina, J.M., Yvin, J.C. and Etienne, P. 2014. Copper-deficiency in Brassica napus induces copper remobilization, molybdenum accumulation and modification of the expression of chloroplastic proteins. PLoS One, 9(10): e109889.
• Bhaduri, D., Rakshit, R. and Chakraborty, K. 2014. Primary and secondary nutrients-a bon to defense system against plant disease. International Journal of Bio-resources and Stress Management, 5: 461-466.
• Bollig, K., Specht, A., Myint, S.S., Zahn, M. and Horst, W.J. 2013. Sulphur supply impairs spread of Verticillium dahliae in tomato. European Journal of Plant Pathology, 135: 81-96.
• Brauer, E.K., Ahsan, N., Dale, R., Kato, N., Coluccio, A.E., Piñeros, M.A., Kochian, L.V., Thelen, J.J. and Popescu, S.C. 2016. The raf-like kinase ILK1 nd the high affinity K+ transporter HAK5 are required for innate immunity and abiotic stress response. Plant Physiology, 171(2): 1470-1484.
• Briat, J.F., Rouached, H., Tissot, N., Gaymard, F. and Dubos, C. 2015. Integration of P, S, Fe and Zn nutrition signals in Arabidopsis thaliana: potential involvement of PHOSPHATE STARVATION RESPONSE 1 (PHR1). Frontiers in Plant Science, 6: 290.
• Brouwer, S.M., Lindqvist-Reis, P., Persson, D.P., Marttila, S., Grenville-Briggs, L.J. and Andreasson. E. 2021. Visualising the ionome in resistant and susceptible plant-pathogen interactions. Plant Journal, 108: 870-885.
• Brown, P.H., Çakmak, I. and Zhang, Q. 1993. Form and function of zinc in plants: Zinc in Soils and Plants, Ed.: Robson A.D., Springer, Netherlands, Dordrecht, pp: 93-106.
• Burnell, J.N. 1988. The biochemistry of manganese in plants: Manganese in Soils and Plants, Ed.: Graham, R.D., Hannam R.J., Uren N.C., Springer, Dordrecht, pp: 125-137.
• Camacho-Cristóbal, J.J., Rexach, J. and Gonzáles-Fontes, A. 2008. Boron in plants: deficiency and toxicity. Journal of Integrative Biology, 50: 1247-1255.
• Campos, A., van Dijk, W., Ramakrishna, P., Giles, T., Korte, P., Douglas, A., Smith, P. and Salt, D.E. 2021. 1,135 ionomes reveal the global pattern of leaf and seed mineral nutrient and trace element diversity in Arabidopsis thailana. The Plant Journal: for Cell and Molecular Biology, 106(2): 536-554.
• Cesco, S., Tolotti, A., Nadalini, S., Rizzi, S., Valentinuzzi, F., Mimmo, T., Porfido, C., Allegretta, I., Giovannini, O., Perazzolli, M., Cipriani, G., Terzano, R., Pertot, I. and Pii, Y. 2020. Plasmopara viticola infection affects mineral elements allocation and distribution in Vitis vinifera leaves. Scientific Reports, 10(1): 18759.
• Chase, A.R. 1989. Effect of nitrogen and potassium fertilizer rates in severity of Xanthomonas blight of Syngonium podophyllum. Plant Disease, 73(12): 972-975.
• Chu, C., Huang, R., Liu, L., Tang, G., Xiao, J., Yoo, H. and Yuan, M. 2022. The rice heavy-metal transporter OsNRAMP1 regulates disease resistance by modulating ROS homoeostasis. Plant Cell & Environment, 45(4): 1109-1126.
• Clarkson, D.T. and Marschner, H. 1996. Mineral Nutrition of Higher Plants. Second edition, 889 pp; London: Academic Press, Annals of Botany, 78(4): 527-528.
• Cobine, P.A., Cruz, L.F., Navarrete, F., Duncan, D., Tygart, M. and de la Fuente, L. 2013. Xylella fastidiosa differentially accumulates mineral elements in biofilm and planktonic cells. PLoS One, 8: e54936.
• Courbet, G., D'Oria, A., Lornac, A., Diquélou, S., Pluchon, S., Arkoun, M., Koprivova, A., Kopriva, S., Etienne, P. and Ourry, A. 2021. Specificity and plasticity of the functional ionome of Brassica napus and Triticum aestivum subjected to macronutrient deprivation. Frontiers in Plant Science, 12: 64148.
• D’Attoma, G., Morelli, M., Saldarelli, P., Saponari, M., Giampetruzzi, A., Boscia, D., Savino, V.N., De La Fuente, L. and Conine, P.A. 2019. Ionomic differences between susceptible and resistant olive cultivars infected by Xylella fastidiosa in the outbreak areas of Salento, Italy. Pathogens, 8(4): 272.
• Datnoff, L.E., Elmer, W.H. and Huber, D.M. 2007. Mineral nutrition and plant disease. American Phytopathological Society, St Paul, Minnesota, USA, 278p.
• De La Fuente, L., Parker, J.K., Oliver, J.E., Granger, S., Brannen, P.M., van Santen, E. and Cobine, P.A. 2013. The bacterial pathogen Xylella fastidiosa affects the leaf ionome of plant hosts during infection. PLoS One, 8: e62945.
• Del Coco, L., Migoni, D., Girelli, C.R., Angilè, F., Scortichini, M. and Fanizzi, F.P. 2020. Soil and leaf ionome heterogeneity in Xylella fastidiosa subsp. pauca-infected, non-infected and treated olive groves in Apuli, Italy. Plants (Basel, Switzeland), 9(6): 760.
• Deng, F., Yamaji, N., Xia, J. and Ma, J.F. 2013. A member of the heavy metal P-type ATPase OsHMA5 in involved in xylem loading of copper in rice. Plant Physiology, 163: 1353-1362.
• Dimkpa, C.O. and Bindraban, P.S. 2015. Fortification of micronutrients for efficient agronomic production: a review. Agronomy for Sustainable Development, 36: 1-27.
• Dinkeloo, K., Boyd, S. and Pilot, G. 2018. Update on amino acid transporter functions and on possible amino acid sensing mechanisms in plants. Seminars in Cell & Developmental Biology, 74: 105-113.
• Dordas, C. 2009. Role of nutrients in controlling plant diseases in sustainable agriculture: A review. Agronomy for Sustainable Development, 28: 33-46.
• D'Oria, A., Courbet, G., Lornac, A., Pluchon, S., Arkoun, M., Maillard, A., Etienne, P., Diquélou, S. and Ourry, A. 2021. Specificity and plasticity of the functional ionome of Brassica napus and Triticum aestivum exposed to micronutrient or beneficial nutrient deprivation and predictive sensitivity of the ionomic signatures. Frontiers in Plant Science, 12: 641678.
• Elmer, W.H. and Datnoff, L.E. 2014. Mineral nutrition and suppression of plant disease: Encyclopedia of Agriculture and Food Systems, Ed.: Neal V.A., San Diego, Elsevier, pp: 231-244.
• Eren, E. and Argüello, J.M. 2004. Arabidopsis HMA2, a divalent heavy metal- transporting PIB-type ATPase, is involved in cytoplasmic Zn2+ homeostasis. Plant Physiology, 136: 3712-3723.
• Fones, H., Davis, C.A.R., Rico, A., Fang, F., Smith, J.A.C. and Preston, G.M. 2010. Metal hyperaccumulation armors plants against disease. PLoS Pathogens, 6: e1001093.
• Fones, H.N. and Preston, G.M. 2012. Reactive oxygen and oxidative stress tolerance in plant pathogenic Pseudomonas. Fems Microbiology Letters, 327: 1-8.
• Forsberg, S.K., Andreatta, M.E., Huang, X.Y., Danku, J., Salt, D.E. and Carlborg, Ö. 2015. The multi-allelic genetic architecture of a variance-heterogeneity locus for molybdenum concentration in leaves acts as a source of unexplained additive genetic variance. PLoS Genetics, 11(11): e1005648.
• Gao, Y.Q., Chen, J.G., Chen, Z.R., An, D., Lv, Q.Y., Han, M.L., Wang, Y.L., Salt, D.E. and Chao, D.Y. 2017. A new vesicle trafficking regulator CTL1 plays a crucial role in ion homeostasis. PLoS Biology, 15(12): e2002978.
• Garcia-Molina, A., Andrés-Colás, N., Perea-García, A., Neumann, U., Dodani, S.C., Huijser, P., Penarrubia, L. and Puig, S. 2013. The Arabidopsis COPT6 transport protein functions in copper distribution under copperdeficient conditions. Plant and Cell Physiology, 54(8): 1378-1390.
• Ghanta, S., Bhattacharyya, D., Sinha, R. and Banerjee, A. 2011. Nicotiana tabaccum overexpressing –ECS exhibits biotic stress tolerance likely through NPR1-dependent salicyclic acid-mediated pathway. Planta, 233: 895-910.
• Gravot, A., Lieutaud, A., Verret, F., Auroy, P., Vavasseur, A. and Richaud, P. 2004. AtHMA3, a plant P1BATPase, functions as a Cd/Pb transporter in yeast. FEBS Letters, 561: 22-28.
• Guan, S., Xu, Q., Ma, D., Zhang, W., Xu, Z., Zhao, M. and Guo, Z. 2019. Transcriptomics profiling in response to cold stress in cultivated rice and weedy rice. Gene, 685: 96-105.
• Gupta, S.K., Rai, A.K., Kanwar, S.S. and Sharma, T.R. 2012. Comparative analysis of zinc finger proteins involved in plant disease resistance. PLoS ONE, 7: 8.
• Hall, J.A. and Williams, L.E. 2003. Transition metal transporters in plants. Journal of Experimental Botany, 54: 2601-2613.
• Han, Y., Chaouch, S., Mhamdi, A., Queval, G., Zechmann, B. and Noctor, G. 2013. Functioanl analysis of Arabidopsis mutants points to novel roles for glutathione in coupling H2O2 to activation of salicyclic acid accumulation and signaling. Antioxidants and Redox Signaling, 18: 2106-2121.
• Hawkesford, M., Horst, W., Kichey, T., Lambers, H., Schjoerring, J., Møller, I.S. and White, P. 2012. Functions of Macronutrients: Marschner’s mineral nutrition of higher plants. Eds.: Marschner, P., San Diego, USA, Elsevier, pp: 135-189.
• Hennigar, S.R. and McClung, J.P. 2016. Nutritional Immunity: Starving pathogens of trace minerals. American Journal of Lifestyle Medicine, 10(3): 170-173.
• Hindt, M.N., Akmakjian, G.Z., Pivarski, K.L., Punshon, T., Baxter, I., Salt, D.E. and Guerinot, M.L. 2017. BRUTUS and its paralogs, BTS LIKE1 and BTS LIKE2, encode important negative regulators of th iron deficiency response in Arabidopsis thaliana. Metallomics: Integrated Biometal Science, 9(7): 876-890.
• Hoegen, E., Ströberg, A., Pihlgren, U. and Kombrink, E. 2002. Primary structure and tissue-specific expression of the pathogenesis-related protein PR-1b in potato. Molecular Plant Pathology, 3(5): 329-345.
• Hoekenga, O.A., Maron, L.G., Piñeros, M.A., Cançado, G.M., Shaff, J., Kobayashi, Y., Ryan, P.R., Dong, B., Delhaize, E., Sasaki, T., Matsumoto, H., Koyama, H. and Kochian, L.V. 2006. AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. Proceedings of the National Academy of Science of the United States of America, 103: 9738-9743.
• Hoffland, E., Jeger, M.J. and van Beusichem, M.L. 2000. Effect of nitrogen supply rate on disease resistance in tomato depends on the pathogen. Plant and Soil, 218: 239-247.
• Holzmueller, E,J., Jose, S. and Jenkins, M.A. 2007. Influence of calcium, potassium and magnesium on Cornus florida L. density and resistance to dogwood anthracnose. Plant Soil, 290: 189-199.
• Huang, X.Y., Deng, F., Yamaji, N., Pinson, S.R.M., Fujii-Kashino, M., Danku, J., Douglas, A., Guerinot, M.L., Salt, D.E. and Ma, J.F. 2016. A heavy metal P-type ATPase OsHMA4 prevents copper accumulation in rice grain. Nature Communications, 7: 12138.
• Huber, D.M. and Haneklaus, S. 2007. Managing nutrition to control plant disease. Landbauforschung Volkenrode, 57: 313-322.
• Kaiser, B.N., Gridley, K.L., Brady, J.N., Phillips, T. and Tyerman, S.D. 2005. The role of molybdenum in agricultural plant production. Annals of Botany, 745-754.
• Kamiya, T., Borghi, M., Wang, P., Danku, J.M., Kalmbach, L., Hosmani, P.S., Naseer, S., Fujiwara, T., Geldner, N. and Salt, D.E. 2015. The MYB36 transcription factor orchestrates Casparian strip formation. Proceedings of the National Academy of Sciences of the United States of America, 112(33): 10533-10538.
• Karapınar, H.S. ve Kılıçel, F. 2020. Determination of some toxic elements (Cr, Cd, Cu and Pb) Levels in cumin and cinnamon aromatic plants Frequently used as foodstuff. Bursa Uludağ Üniversitesi Ziraat Fakültesi Dergisi, 34: 1-8.
• Kieu, N.P., Anzar, A., Segond, D., Rigault, M., Simond-Côte, E., Kunz, C., Soulie, M.C., Expert, D. and Dellagi, A. 2012. Iron deficiency affects plant defence responses and confers resistance to Dickeya dadantii and Botrytis cinerea. Molecular Plant Pathology, 13(8): 816-827.
• Kim, S.H., Hong, J.K., Lee, S.C., Sohn, K.H., Jung, H.W. and Hwang, B.K. 2004. CAZFP1, CYS2/HİS(2)-type zinc-finger transcription factor gene functions as a pathogen-induced early-defense gene in Capsicum annuum. Plant Molecular Biology, 55: 883-904.
• Kobayashi, T., Nagasaka, S., Senoura, T., Itai, R.N., Nakanishi, H. and Nishizawa, N.K. 2013. Iron-binding haemerythrin RING ubiquitin ligases regulate plant iron responses and accumulation. Nature Communications, 4: 2792.
• Kobayashi, T., Nozoye, T. and Nishizawa, N.K. 2019. Iron transport and its regulation in plants. Free Radical Biology and Medicine, 133: 11-20.
• 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.
• Kronzucker, H.J., Coskun, D., Schulze, L.M., Wong, J.R. and Britto, D.T. 2013. Sodium as nutrient and toxicant. Plant Soil, 369: 1-23.
• Kruse, C., Haas, F.H., Jost, R., Reiser, B., Reichelt, M., Wirtz, M., Gershenzon, J., Schnug, E. and Hell, R. 2012. Improved sulfur nutrition provides the basis for enhanced production of sulfur-containing defense compounds in Arabidopsis thaliana upon inoculation with Alternaria brassicicola. Journal of Plant Physiology, 169: 740-743.
• Kudla, J., Batistic, O. and Hashimoto, K. 2010. Calcium signals: The lead currency of plant information processing. Plant Cell, 22: 541-563.
• Lahner, B., Gong, J., Mahmoudian, M., Smith, E.L., Abid, K.B., Rogers, E.E., Guerinot, M.L., Harper, J.F., Ward, J.M., Mclntyre, L., Schroeder, J.I. and Salt, D.E. 2003. Genomic scale profiling of nutrient and trace elements in Arabidopsis thaliana. Nature Biotechnology, 21(10): 1215-1221.
• Li, N., Liu, H., Sun, J., Zheng, H., Wang, J., Yang, L., Zhao, H. and Zou, D. 2018. Transcriptome analysis of two contrasting rice cultivars during alkaline stress. Scientific Reports, 8(1): 1-16.
• Liu, S., Zhong, H., Meng, X., Sun, T., Li, Y., Pinson, S.R., Chang, S,K. and Peng, Z. 2020. Genome-wide association studies of ionomic and agronomic traits in USDA mini core collection of rice and comparative analyses of different mapping methods. BMC Plant Biology, 20: 441.
• Lopez-Delacalle, M., Camejo, D.M., García-Martí, M., Nortes, P.A., Nieves-Cordones, M., Martínez, V., Rubio, F., Mittler. R. and Rivero, R.M. 2020. Using tomato recombinant lines to improve plant tolerance to stress combination through a more efficient nitrogen metabolism. Frontiers of Plant Science, 10: 1702.
• Maathuis F.J. 2009. Pyhsiological functions of mineral macronutrients. Current Opinion in Plant Biology, 12(3): 250-258.
• Mann, A., Singh, S., Kumar, A., Kumar, S. and Kumar, B. 2018. Plant ionomics: an important component of functional biology: Metabolic Adaptations in Plant During Abiotic Stress, Ed.: Ramakrishna, A., Gill S.S., . CRC Press, pp: 147-154.
• Marschner, H. 2012. Marschner’s mineral nutrition of higher plants (No. Ed. 3). Elsevier, London, 649p.
• Maser, P., Thomine, S., Schroeder, J.I., Ward, J.M., Hirschi, K., Sze, H., Talke, I.N., Amtmann, A., Maathuis, F.J. and Sanders, D. 2001. Phylogenetic relationship within cation transporter families of Arabidopsis. Plant Physiology, 126: 1646-1667.
• Mendel, R.R. 2011. Cell biology of molybdenum in plants. Plant Cell Reports, 30(10): 1787-1797.
• Millaleo, R., Reyes-Diaz, M., Ivanov, A., Mora, M. and Alberdi, M. 2010. Manganese as essential and toxic element for plants: transport, accumulation and resistance mechanisms. The Journal of Soil Science and Plant Nutrition, 10(4): 470-481.
• Mills, R.F., Krijger, G.C., Baccarini, P.J., Hall, J.L. and Williams, L.E. 2003. Functional expression of AtHMA4, a P1B-type ATPase of the Zn/Co/Cd/Pb subclass. Plant Journal. 35: 164-176.
• Mills, R.F., Krijger, G.C., Baccarini P.J., Hall, J.L. and Williams, L.E. 2005. The plant P1B-type ATPase AtHMA4 transports Zn and Cd and plays a role in detoxification of transition metals supplied at elevated levels. FEBS Letters, 579: 783-791.
• Misra, B.B., Reichman, S.M. and Chen, S. 2019. The guard cell ionome: understanding the role of ions in guard cell functions. Progress in Biophysics and Molecular Biology, 146: 50-62.
• Miyamoto-Maeta, M., Kamiya, T., Fujiwara, T., Hirotomi, D. and Iwata, H. 2021. Time-course changes in the ionomic profile of rice leaves and their application in growth stage prediction. Crop Science, 61: 4239-4254.
• 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: 107.
• Morel, M., Crouzet, J., Gravot, A., Auroy, P., Leonhardt, N., Vavasseur, A. and Richaud, P. 2009. AtHMA3, a P1B-ATPase allowing Cd/Zn/co/Pb vacuolar storage in Arabidopsis. Plant Physiology, 149: 894-904.
• Navarrete, F. and De La Fuente, L. 2015. Zinc detoxification is required for full virulence and modification of the host leaf ionome by Xylella fastidiosa. Molecular Plant-Microbe Interactions, 28: 497-507.
• Nicolas, O., Charles, M.T., Jenni, S., Taussaint, V., Parent, S.É. and Beaulieu, C. 2019. The ionomics of lettuce infected by Xanthomonas campestris pv. vitians. Frontiers in Plant Science, 10: 351.
• Outten, C.E. and O’Halloran, T.V. 2001. Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science (New York, NY), 292(5526): 2488-2492.
• Pais, I. and Jones, Jr J.B. 1997. The handbook of trace elements (No. Ed. 1). CRC Press, Boca Raton, FL, USA, 240p.
• Payne, K.A., Bowen, H.C., Hammond, J.P., Hampton, C.R., Lynn, J.R., Mead, A., Swarup, K., Bennett, M.J., White, P.J. and Broadly, M.R. 2004. Natural genetic variation in caesium (Cs) accumulation by Arabidopsis thaliana. New Phytologist, 162: 535-548.
• Pierre, J.L. and Fontecave, M. 1999. Iron and activated oxygen species in biology: The basic chemistry. Biometals, 12: 195-199.
• Pilon-Smits, E.A., Quinn, C.F., Tapken, W., Malagoli, M. and Schiavon, M. 2009. Physiological functions of beneficial elements. Current Opinion in Plant Biology, 12(3): 267-274.
• Pita-Barbosa, A., Ricachenevsky, F.K., Wilson, M., Dottorini, T. and Salt, D.E. 2019. Transcriptional Plasticity Buffers Genetic Variation in Zinc Homeostasis. Scientific Reports, 9: 19482.
• Poschenrieder, C., Tolrà, R. and Barceló, J. 2006. Can metals defend plants against biotic stress? Trends in Plant Science, 11: 288-295.
• Poormohammad, Kiani S., Trontin, C., Andreatta, M., Simon, M., Robert, T., Salt, D.E. and Loudet, O. 2012. Allelic heterogeneity and trade-off shape natural variation for response to soil micronutrient. PLoS Genetics, 8(7): e1002814.
• Quan, X., Zeng, J., Han, Z. and Zhang, G. 2017. Ionomic and physiological responses to low nitrogen stress in Tibetan wild and cultivated barley. Plant Pyhsiology and Biochemistry: PPB, 111: 257-265.
• Rai, W., Khatoon, S., Bisht, S.S. and Mehrotra, S. 2005. Effect of cadmium on growth, ultramorfology of leaf and secondary metabolites of Phyllanthus amarus Schum. and Thonn. Chemosphere, 61: 1644-1650.
• Rasoolizadeh, A., Labbé, C., Sonah, H., Deshmukh, R.K., Belzile, F., Menzies, J.G. and Bélanger, R.R. 2018. Silicon protects soybean plants against Phytophthora sojae by interfering with effector-receptor expression. BMC Plant Biology, 18(1): 1-13.
• Rauh, L., Basten, C. and Buckler, S., 4th. 2002. Quantitative trait loci analysis of growth response to varying nitrogen sources in Arabidopsis thaliana. Theoritical and Applied Genetics, 104(5): 743-750.
• Rodríguez-Jiménez, T.D.J., Ojeda-Barrios, D.L., Blanca-Macíos, F., Valdez-Cepeda, R.D. and Parra-Quezada, R. 2016. Urease y niquel en la fisiologia de las plantas. Revista Chapingo, Serie Horticultura, 22(2): 69-82.
• Sasaki, A., Yamaji, N. and Ma, J.F. 2016. Transporters involved in mineral nutrient uptake in rice. Journal of Experimental Botany, 67: 3645-3653.
• Satismruti, K., Senthil, N., Vellaikumar, S., Ranjani, R.V. and Raveendran, M. 2013. Plant ionomics: a platform for identifying novel gene regulating plant mineral nutrition. American Journal of Plant Sciences, 4: 1309- 1315.
• Sebastiani, L., Scebba, F. and Tognetti, R. 2004. Heavy metal accumulation and growth responses in poplar clones Eridano (Populus deltoides × maximowiczii) and I-214 (P. × euramericana) exposed to industrial waste. Environmental and Experimental Botany, 52: 79-88.
• Sharma, E., Jain, M. and Khurana, J.P. 2019. Differential quantitative regulation of specific gene groups and pathways under drought stress in rice. Genomics, 111(6): 1699-1712.
• Shen, C., Yang, Y., Liu, K., Zhang, L., Guo, H., Sun, T. and Wang, H. 2016. Involvement of endogenous salicyclic acid in iron-deficiency responses in Arabidopsis. Journal of Experimental Botany, 67(14): 4179- 4193.
• Singh, S., Parihar, P., Singh, R., Singh, V.P. and Prasad, S.M. 2016. Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics and ionomics. Frontiers of Plant Science, 6: 1143.
• Singh, A., Jaiswal, A., Singh, A., Tomar, R.S. and Kumar, A. 2021. Plant ionomics: toward high-throughput nutrient profiling: Plant Nutrition and Food Security in the Era of Climate Change, Ed.: Kumar, V., Srivastava, A.K., Suprasanna, P., Elsevier/Academic Press, pp. 227-254.
• Spann, T.M. and Schumann, A.W. 2010. Mineral nutrition contributes to plant disease and pest resistance. One of the Series of the Horticultural Sciences Department, Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida, IFAS Extension, This document is HS1181. http://edis.ifas.ufl.edu
• Sun, X., Pan, B., Wang, Y., Xu, W. and Zhang, S. 2020. Exogenous calcium improved resistance to Botryosphaeria dothidea by increasing autophagy activity and salicyclic acid level in pear. Molecular PlantMicrobe Interactions, 33: 1150-1160.
• Suzuki, M., Bashir, K., Inoue, H., Takahashi, M., Nakanishi, H. and Nishizawa, N.K. 2012. Accumulation of starch in Zinc-deficient rice. Rice, 5: 9.
• Szpunar, J. 2004. Metallomics: a new frontier in analytical chemistry. Analytical and Bioanalytical Chemistry, 378(1): 54-56.
• Takahashi, R., Bashir, K., Ishimaru, Y., Nishizawa, N.K. and Nakanishi, H. 2012a. The role of heavy-metal ATPases, HMAs, in zinc and cadmium transport in rice. Plant Signaling and Behavier, 7: 1506-1607.
• Takahashi, R., Ishimaru, Y., Shimo, H., Ogo, Y., Senoura, T., Nishizawa, N.K. and Nakanishi, H. 2012b. The OsHMA2 transporter is involved in root-to-shoot translocation of Zn and Cd in rice. Plant Cell and Environment, 35: 1948-1957.
• Terranova, M.L. and Tavares, O.A.P. 2022. The periodic table of the elements: the search for transactinides and beyond. Rendiconti Lincei-Scienze Fisiche E Naturali, 33: 1-16.
• Thapa, G., Sadhukhan, A., Panda, S.K. and Sahoo, L. 2012. Molecular mechanistic model of plant heavy metal tolerance. Biometals, 25(3): 489-505.
• 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.
• Thor, K. 2019. Calcium-nutrient and Messenger. Frontiers in Plant Science, 10: 440.
• Torres, M.A. 2010. ROS in biotic interactions. Physiologia Plantarum, 138: 414-429.
• Usmani, M.M., Nawaz, F. and Majeed, S. 2020. Sulfate-mediated drought tolerance in maize involves regulation at physiological and biochemical levels. Scientific Reports, 10: 1147.
• Veley, K.M., Berry, J.C., Fentress, S.J., Schachtman. D.P., Baxter, I. and Bart, R. 2017. High-throughput profiling and analysis of plant responses over time to abiotic stress. Plant Direct, 1: e00023.
• Verret, F., Gravot, A., Auroy, P., Preveral, S., Forestier, C., Vavasseur, A. and Richaud, P. 2005. Heavy metal transport by AtHMA4 involves the N-terminal degenerated metal binding domain and the C-terminal His11 strech. FEBS Letters, 579: 1515-1522.
• Walters, D.R. and Bingham, I.J. 2007. Influence of Nutrition on Disease Development Caused by Fungal Pathogens: Implications for Plant Disease Control. Annals of Applied Biology, 151: 307-324.
• Wang, M., Gao, L., Dong, S., Sun, Y., Shen, Q. and Guo, S. 2017. Role of silicon on plant- pathogen interactions. Frontiers in Plant Science, 8: 701.
• Watanabe, T., Urayana, M., Shinano, T., Okada, R. and Osaki, M. 2015. Application of ionomics to plant and soil in fields under long-term fertilizer trials. SpringerPlus, 4: 781.
• Watanabe, T., Okada, R. and Urayama, M. 2022. Differences in ionomic responses to nutrient deficiencies among plant species under field conditions. Journal of Plant Nutrition, 45(10): 1493-1503.
• Whitt, L., Ricachenevsky, F.K., Ziegler, G.Z., Clemens, S., Walker, E., Maathuis, F., Kear, P. and Baxter, I. 2020. A curated list of genes that affect the plant ionome. Plant Direct, 4(10): e00272.
• Williams, R.J.P. 2001. Chemical selection of elements by cells. Coordination Chemistry Reviews, 216: 583-595.
• Xuan, Y.H., Hu, Y.B., Chen, L.Q., Sosso, D., Ducat, D.C., Hou, B.H. and Frommer, W.B. 2013. Functional role of oligomerization for bacterial and plant SWEET sugar transporter family. Proceedings of the National Academy of Sciences of the United States of America, 110(39): E3685-E3694.
• Yadeta, K.A., Elmore, J.M., Creer, A.Y., Feng, B., Franco, J.Y., Rufian, J.S., He, P., Phinney, B. and Coaker, G. 2017. A cysteine-rich protein kinase associates with a membrane immune complex and cysteine residues are required for cell death. Plant Physiology, 173: 771-787.
• Yang, M., Lu, K., Zhao, F.J., Xie, W., Ramakrishna, P., Wang, G., Du, Q., Liang, L., Sun, C., Zhao, H., Zhang, Z., Liu, Z., Tian, J., Huang, X.Y., Wang, W., Dong, H., Hu, J., Ming, L., Xing, Y.,Wang, G., Xiao, J., Salt, D.E. and Lian, X. 2018. Genome-wide association studies reveal the genetic basis of ionomic variation in rice. The Plant Cell, 30(11): 2720-2740.
• Yasin, N.A., Zheer, M.M., Khan, W.U., Ahmad, S.R., Ali, A. and Akram, W. 2018. The beneficial role of potassium in Cd-induced stress alleviation and growth improvement in Gladiolus grandiflora L. International Journal of Phytoremediation, 20: 274-283.
• Yruela, I. 2005. Copper in plants. Brazilian Journal of Plant Physiology, 17: 145-156.
• Yuan, M., Wang, S., Chu, Z., Li, X. and Xu, C. 2010. The bacterial pathogen Xanthomonas oryzae overcomes rice defenses by regulating host copper redistribution. Plant Cell, 22: 3164-3176.
• Zhao, H., Sun, R., Albrecht, U., Padmanabhan, C., Wang, A., Coffey, M.D., Girke, T., Wang, Z., Close, T.J., Roose, M., Yokomi, R.K., Folimonova, S., Vidalakis, G., Rouse, R., Bowman, K.D. and Jin, H. 2013. Small RNA profiling reveals phosphorus deficiency as a contributing factor in symptom expression for citrus huanglongbing disease. Molecular Plant, 6(2): 301-310.