Abstract
Selenium (Se) is an essential nutrient for many organisms but is toxic at high levels. A better understanding of plant responses to Se is important to optimize the use of plants in alleviating dietary Se deficiency or for the cleanup of Se-polluted areas. Genetic analysis among accessions of Arabidopsis thaliana showed that several genes involved in sulfur (S) assimilation may be responsible for the differences in Se resistance and accumulation, and resistance to selenite and selenate may be regulated by different genes. Molecular and biochemical studies of non-accumulator plants revealed that defense responses mediated by phytohormones (such as ethylene, jasmonic acid, and salicylic acid) play an important role in acquiring Se resistance and accumulation. Production of these phytohormones is enhanced via signal pathways of reactive oxygen species (ROS), and the signal pathways of phytohormones act in a cooperative or antagonistic manner to induce stress and S-uptake and S-metabolic genes. In this chapter, the contribution of ROS and phytohormone signaling in the acquisition of Se resistance and accumulation in Se hyper-accumulator plants was discussed, and the application of Se-responsive genes to generate transgenic plants that can detect Se in the environment was also introduced.
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Cao H, Glazebrook J, Clarke JD, Volko S, Dong X (1997) The Arabidopsis NPR1 gene that control systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88:57–63
Clarke JD, Volko SM, Ledford H, Ausubel FM, Dong X (2000) Roles of salicylic acid, jasmonic acid, and ethylene in cpr-induced resistance in Arabidopsis. Plant Cell 12:2175–2190
Correa-Aragunde N, Graziano M, Chevalier C, Lamattina L (2006) Nitric oxide modulates the expression of cell cycle regulatory genes during lateral root formation in tomato. J Exp Bot 57:581–588
De Bruyne L, Höfte M, De Vleesschauwer D (2014) Connecting growth and defense: the emerging roles of brassinosteroids and gibberellins in plant innate immunity. Mol Plant 7:943–959
Denancé N, Sánchez-Vallet A, Goffner D, Molina A (2013) Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs. Front Plant Sci 4:155
de Souza MP, Pilon-Smits EAH, Lytle CM, Hwang S, Tai JC, Honma TSU, Yeh L, Terry N (1998) Rate-limiting steps in selenium volatilization by Brassica juncea. Plant Physiol 117:1487–1494
Dong X (1998) SA, JA, ethylene, and disease resistance in plants. Curr Opin Plant Biol 1:316–323
Durner J, Shah J, Klessig DF (1997) Salicylic acid and disease resistance in plants. Trends Plant Sci 2:162–165
Ellis DR, Sors TG, Brunk DG, Albrecht C, Orser C, Lahner B, Wood KV, Harris HH, Pickering IJ, Salt DE (2004) Production of Se-methylselenocysteine in transgenic plants expressing selenocysteine methyltransferase. BMC Plant Biol 4:1–11
Eustice DC, Kull FJ, Shrift A (1981) Selenium toxicity: aminoacylation and peptide bond formation with selenomethionine. Plant Physiol 67:1054–1058
Feechan A, Kwon E, Yun B-W, Wang Y, Pallas JA, Loake GJ (2005) A central role for S-nitrosothiols in plant disease resistance. Proc Nat Acad Sci USA 102:8054–8059
Feng J, Wang C, Chen Q, Chen H, Ren B, Li X, Zuo J (2013) S-nitrosylation of phosphotransfer proteins represses cytokinin signaling. Nat Commun 4:152910
Freeman JL, Zhang LH, Marcus MA, Fakra S, McGrath SP, Pilon-Smits EAH (2006) Spatial imaging, speciation and quantification of selenium in the hyperaccumulator plants Astragalus bisulcatus and Stanleya pinnata. Plant Physiol 142:124–134
Freeman JL, Tamaoki M, Stushnoff C, Quinn CF, Cappa JJ, Devonshire J, Fakra SC, Marcus MA, McGrath SP, Van Hoewyk D, Pilon-Smits EAH (2010) Molecular mechanisms of selenium tolerance and hyperaccumulation in Stanleya pinnata. Plant Physiol 153:1630–1652
Gomes-Jr RA, Gratão PL, Gaziola SA, Mazzafera PM, Lea PJ, Azevedo RA (2007) Selenium-induced oxidative stress in coffee cell suspension cultures. Funct Plant Biol 34:449–456
Gromer S, Gross JH (2002) Methylseleninate is a substrate rather than an inhibitor of mammalian thioredoxin reductase. Implications for the antitumor effects of selenium. J Biol Chem 277:9701–9706
Gupta V, Willits MG, Glazebrook J (2000) Arabidopsis thaliana EDS4 contributes to salicylic acid (SA)-dependent expression of defense responses: evidence for inhibition of jasmonic acid signaling by SA. Mol Plant-Microbe Interact 13:503–511
Guzmán P, Ecker JR (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2:513–523
Hamilton SJ (2004) Review of selenium toxicity in the aquatic food chain. Sci Total Environ 326:1–31
Hansen D, Duda PJ, Zayed AM, Terry N (1998) Selenium removal by constructed wetlands: role of biological volatilization. Environ Sci Technol 32:591–597
Hira CK, Partal K, Dhillon K (2004) Dietary selenium intake by men and women in high and low selenium areas of Punjab. Public Health Nutr 7:39–43
Kachroo P, Shanklin J, Shah J, Whittle EJ, Klessig DF (2001) A fatty acid desaturase modulates the activation of defense signaling pathways in plants. Proc Natl Acad Sci USA 98:9448–9453
Kassis EE, Cathala N, Rouached H, Fourcroy P, Berthomieu P, Terry N, Davidian JC (2007) Characterization of a selenate-resistant Arabidopsis mutant. Root growth as a potential target for selenate toxicity. Plant Physiol 143:1231–1241
Kawashima CG, Matthewman CA, Huang S, Lee BR, Yoshimoto N, Koprivova A, Rubio-Somoza I, Todesco M, Rathjen T, Saito K, Takahashi H, Dalamay T, Kopriva S (2011) Interplay of SLIM1 and miR395 in the regulation of sulfate assimilation in Arabidopsis. Plant J 66:863–876
Kazan K, Lyons R (2014) Intervention of phytohormone pathways by pathogen effectors. Plant Cell 26:2285–2309
Keller T, Damude HG, Werner D, Doerner P, Dixon RA, Lamb C (1998) A plant homologue of the neutrophil NADPH oxidase gp91 phox subunit gene encodes a plasma membrane protein with Ca2+ binding motifs. Plant Cell 10:255–266
Kloek AP, Verbsky ML, Sharma SB, Schoelz JE, Vogel J, Klessig DF, Kunkel BN (2001) Resistance to Pseudomonas syringae conferred by an Arabidopsis thaliana coronatine-insensitive (coi1) mutation occurs through two distinct mechanisms. Plant J 26:509–522
Kovalchuk O, Titov V, Hohn B, Kovalchuk I (2001) A sensitive transgenic plant system to detect toxic inorganic compounds in the environment. Nat Biotechnol 19:568–572
Krizek BA, Prost V, Joshi RM, Stoming T, Glenn TC (2003) Developing transgenic Arabidopsis plants to be metal-specific bioindicators. Environ Toxicol Chem 22:175–181
Läuchli A (1993) Selenium in plants: uptake, functions, and environmental toxicity. Bot Acta 106:455–468
Lawton KA, Potter SL, Uknes S, Ryals J (1994) Acquired resistance signal transduction in Arabidopsis is ethylene independent. Plant Cell 6:581–588
LeDuc DL, Tarun AS, Montes-Bayon M, Meija J, Malit MF, Wu CP, AbdelSamie M, Chiang C-Y, Tagmount A, deSouza MP, Neuhierl B, Böck A, Caruso JA, Terry N (2004) Overexpression of selenocysteine methyltransferase in Arabidopsis and indian mustard increases selenium tolerance and accumulation. Plant Physiol 135:377–383
Lehotai N, Kolbert Z, Petõ A, Feigl G, Ördög A, Kumar D, Tari I, Erdei L (2012) Selenite-induced hormonal and signalling mechanisms during root growth of Arabidopsis thaliana L. J Exp Bot 63:5677–5687
Leslie CA, Romani RJ (1988) Inhibition of ethylene biosynthesis by salicylic acid. Plant Physiol 88:833–837
Lorenzo O, Solano R (2005) Molecular players regulating the jasmonate signaling network. Curr Opin Plant Biol 8:532–540
Mähönen AP, ten Tusscher K, Siligato R, Smetana O, Díaz-Triviño S, Salojärvi J, Wachsman G, Prasad K, Heidstra R, Scheres B (2014) PLETHORA gradient formation mechanism separates auxin responses. Nature 515:125–129
Maruyama-Nakashita A (2016) Combinatorial use of sulfur-responsive regions of sulfate transporters provides a highly sensitive plant-based system for detecting selenate and chromate in the environment. Soil Sci Plant Nutr 62:386–391
Maruyama-Nakashita A, Inoue E, Watanabe-Takahashi A, Yamaya T, Takahashi H (2003) Transcriptome profiling of sulfur-responsive genes in Arabidopsis reveals global effect on sulfur nutrition on multiple metabolic pathways. Plant Physiol 132:597–605
Maruyama-Nakashita A, Nakamura Y, Yamaya T, Takahashi H (2004) A novel regulatory pathway of sulfate uptake in Arabidopsis roots: implication of CRE1/WOL/AHK4-mediated cytokinin-dependent regulation. Plant J 38:779–789
Maruyama-Nakashita A, Inoue E, Saito K, Takahashi H (2007) Sulfur-responsive promoter of sulfate transporter gene is potentially useful to detect and quantify selenate and chromate. Plant Biotechnol 24:261–263
Maruyama-Nakashita A, Watanabe-Takahashi A, Inoue E, Yamaya T, Saito K, Takahashi H (2015) Sulfur-responsive elements in the 3′-nontranscribed intergenic region are essential for the induction of SULFATE TRANSPORTER 2;1 gene expression in Arabidopsis roots under sulfur deficiency. Plant Cell 27:1279–1296
McNeal JM, Balisteri LS (1989) Geochemistry and occurrence of selenium: an overview. Selenium in agriculture and the environment, Special publication no. 23. Soil Science Society of America, Madison
Mirouze M, Sels J, Richard O, Czernic P, Loubet S, Jacquier A, François IEJA, Cammue BPA, Lebrun M, Berthomieu P, Marquès L (2006) A putative novel role for plant defensins: a defensin from the zinc hyper-accumulating plant, Arabidopsis halleri, confers zinc tolerance. Plant J 47:329–342
Neuhierl B, Thanbichler M, Lottspeich F, Böck A (1999) A family of S-methylmethionine-dependent thiol/selenol methyltransferases. Role in selenium tolerance and evolutionary relation. J Biol Inorg Chem 274:5407–5414
Overmyer K, Broschė M, Kangasjärvi J (2003) Reactive oxygen species and hormonal control of cell death. Trends Plant Sci 8:335–342
Overvoorde P, Fukaki H, Beeckman T (2010) Auxin control of root development. Cold Spring Harb Perspect Biol 2:a001537
Penninckx IAMA, Thomma BPHJ, Buchla A, Métraux J-P, Broekaert WF (1998) Concomitant activation of jasmonate and ethylene response pathway is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 10:2103–2114
Petersen M, Brodersen P, Naested H, Andreasson E, Lindhart U, Johansen B, Nielsen HB, Lacy M, Austin MJ, Parker JE, Sharma SB, Klessig DF, Martienssen R, Mattsson O, Jensen AB, Mundy J (2000) Arabidopsis map kinase 4 negatively regulates systemic acquired resistance. Cell 103:1111–1120
Peuke AD, Rennenberg H (2005) Phytoremediation: molecular biology, requirements for application, environmental protection, public attention and feasibility. EMBO Rep 6:497–501
Pieterse CMJ, Leon-Reyes A, Van der Ent S, Van Wees SCM (2009) Networking by small-molecules hormones in plant immunity. Nat Chem Biol 5:308–316
Pilon-Smits EAH (2005) Phytoremediation. Annu Rev Plant Biol 56:15–39
Pilon-Smits EAH, Hwang S, Lytle CM, Zhu YL, Tai JC, Bravo RC, Chen Y, Leustek T, Terry N (1999) Overexpression of ATP sulfurylase in Indian mustard leads to increased selenate uptake, reduction, and tolerance. Plant Physiol 119:123–132
Pilon-Smits EAH, Quinn CF, Tapken W, Malagoli M, Schiavon M (2009) Physiological functions of beneficial elements. Curr Opin Plant Biol 12:267–274
Rouached H, Wirtz M, Alary R, Hell R, Arpat AB, Davidian JC, Fourcroy P, Berthomieu P (2008) Differential regulation of the expression of two high-affinity sulfate transporters, SULTR1.1 and SULTR1.2, in Arabidopsis. Plant Physiol 147:897–911
Rouached H, Secco D, Arpat AB (2009) Getting the most sulfate from soil: regulation of sulfate uptake transporters in Arabidopsis. J Plant Physiol 166:893–902
Salt DE, Smith RD, Raskin I (1998) Phytoremediation. Annu Rev Plant Physiol Plant Mol Biol 49:643–668
Sasaki-Sekimoto Y, Taki N, Obayashi T, Aono M, Matsumoto F, Sakurai N, Suzuki H, Yokota-Hirai M, Noji M, Saito K, Masuda T, Takamiya K, Shibara D, Ohta H (2005) Coordinated activation of metabolic pathway for antioxidants and defence compounds by jasmonates and their roles in stress tolerance in Arabidopsis. Plant J 44:653–668
Shahzad Z, Ranwez V, Fizames C, Marquès L, Le Martret B, Alassimone J, Godé C, Lacombe E, Castillo T, Saumitou-Laprade P, Berthomieu P, Gosti F (2013) Plant Defensin type 1 (PDF1): protein promiscuity and expression variation within the Arabidopsis genus shed light on zinc tolerance acquisition in Arabidopsis halleri. New Phytol 200:820–833
Shibagaki N, Rose A, McDermott JP, Fujiwara T, Hayashi H, Yoneyama T, Davies JP (2002) Selenate-resistant mutants of Arabidopsis thaliana identify Sultr1;2, a sulfate transporter required for efficient transport of sulfate into roots. Plant J 29:475–486
Sors TG, Ellis DR, Salt DE (2005) Selenium uptake, translocation, assimilation and metabolic fate in plants. Photosynth Res 86:373–389
Stadtman TC (1990) Selenium biochemistry. Annu Rev Biochem 59:111–127
Staswick PE, Su W, Howell SH (1992) Methyl jasmonate inhibition of root growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proc Natl Acad Sci USA 89:6837–6840
Stenzel I, Hause B, Miersch O, Kurz T, Mauzher H, Weichert H, Ziegler J, Feussner I, Wasternack C (2004) Jasmonate biosynthesis and the allene oxide cyclase family of Arabidopsis thaliana. Plant Mol Biol 51:895–911
Takahashi H, Yamazaki M, Sasakura N, Watanabe A, Leustek T, Engler JA, Engler G, Van Montagu M, Saito K (1997) Regulation of sulfur assimilation in higher plants: a sulfate transporter induced in sulfate starved roots plays a central role in Arabidopsis thaliana. Proc Natl Acad Sci USA 94:11102–11107
Takahashi H, Watanabe-Takahashi A, Smith FW, Blake-Kalff M, Hawkesford MJ, Saito K (2000) The roles of three functional sulfate transporters involved in uptake and translocation of sulfate in Arabidopsis thaliana. Plant J 23:171–182
Tamaoki M (2008) The role of phytohormone signaling in ozone-induced cell death in plants. Plant Signal Behav 3:166–174
Tamaoki M, Nakajima N, Kubo A, Aono M, Matsuyama T, Saji H (2003) Transcriptome analysis of O3-exposed Arabidopsis reveals that multiple signal pathways act mutually antagonistically to induce gene expression. Plant Mol Biol 53:443–456
Tamaoki M, Freeman JL, Pilon-Smits EAH (2008a) Cooperative ethylene and jasmonic acid signaling regulates selenite resistance in Arabidopsis thaliana. Plant Physiol 146:1219–1230
Tamaoki M, Freeman JL, Marquès L, Pilon-Smits EAH (2008b) New insights into the roles of ethylene and jasmonic acid in the acquisition of selenium resistance in plants. Plant Signal Behav 3:865–867
Terry N, Zayed AM, de Souza MP, Tarun AS (2000) Selenium in higher plants. Annu Rev Plant Physiol Plant Mol Biol 51:401–432
Torres MA, Onouchi H, Hamada S, Machida C, Hammond-Kosack KE, Jones JD (1998) Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp 91phox). Plant J 14:365–370
Van Hoewyk D, Takahashi H, Inoue E, Hess A, Tamaoki M, Pilon-Smits EAH (2008) Transcriptome analyses give insights into selenium-stress responses and selenium tolerance mechanisms in Arabidopsis. Physiol Plant 132:236–253
Vanneste S, Friml J (2009) Auxin: a trigger for change in plant development. Cell 136:1005–1016
Werner T, Nehnevajova E, Köllmer I, Novák O, Strnad M, Krämer U, Schmülling T (2010) Root-specific reduction of cytokinin causes enhanced root growth, drought tolerance, and leaf mineral enrichment in Arabidopsis and tobacco. Plant Cell 22:3905–3920
WHO (2011) Guidelines for drinking-water quality: forth edition. ISBN: 978 92 4 154815 1.
Wilber CG (1980) Toxicology of selenium: a review. Clin Toxicol 17:171–230
Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defense. Nature 414:562–565
Wilkinson JQ, Crawford NM (1993) Identification and characterization of a chlorate resistant mutant of Arabidopsis with mutations in both NIA1 and NIA2 nitrate reductase structural genes. Mol Gen Genet 239:289–297
Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95:707–735
Yalpani N, Enyedi AJ, León J, Raskin I (1994) Ultraviolet light and ozone stimulate accumulation of salicylic acid, pathogenesis-related proteins and virus resistance in tobacco. Planta 193:372–376
Yamaguchi C, Takimoto Y, Ohkama-Ohtsu N, Hokura A, Shinano T, Nakamura T, Suyama A, Maruyama-Nakashita A (2016) Effects of cadmium treatment on the uptake and translocation of sulfate in Arabidopsis thaliana. Plant Cell Physiol 57:2353–2366
Yoshimoto N, Takahashi H, Smith FW, Yamaya T, Saito K (2002) Two distinct high-affinity sulfate transporters with different inducibilities mediate uptake of sulfate in Arabidopsis roots. Plant J 29:465–473
Yoshimoto N, Inoue E, Watanabe-Takahashi A, Saito K, Takahashi H (2007) Posttranscriptional regulation of high-affinity sulfate tansporters in Arabidopsis by sulfur nutrition. Plant Physiol 145:378–388
Zarembinski TI, Theologis A (1994) Ethylene biosynthesis and action: a case of conservation. Plant Mol Biol 26:1579–1597
Zhang LH, Byrne PF, Pilon-Smits EAH (2006a) Mapping quantitative trait loci associated with selenate tolerance in Arabidopsis thaliana. New Phytol 170:33–42
Zhang LH, Abdel-Ghany SE, Freeman JL, Ackley AR, Schiavon M, Pilon-Smits EAH (2006b) Investigation of selenium tolerance mechanism in Arabidopsis thaliana. Physiol Plant 128:212–223
Zhang LH, Ackley AR, Pilon-Smits EAH (2007) Variation in selenium tolerance and accumulation among 19 Arabidopsis thaliana accessions. J Plant Physiol 164:327–336
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Tamaoki, M., Maruyama-Nakashita, A. (2017). Molecular Mechanisms of Selenium Responses and Resistance in Plants. In: Pilon-Smits, E., Winkel, L., Lin, ZQ. (eds) Selenium in plants. Plant Ecophysiology, vol 11. Springer, Cham. https://doi.org/10.1007/978-3-319-56249-0_3
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