Sweet sorghum (Sorghum bicolor L.) SbSTOP1 activates the transcription of a β-1,3-glucanase gene to reduce callose deposition under Al toxicity: A novel pathway for Al tolerance in plants

References

• Uexküll HRV, Mutert E. Global extent, development and economic impact of acid soils. Plant Soil. 1995;171:1–15.
   Web of Science ®Google Scholar
• Guo JH, Liu XJ, Zhang Y, et al. Significant acidification in major Chinese croplands. Science. 2010;327:1008–1010.
   PubMed Web of Science ®Google Scholar
• Kochian LV, Piñeros MA, Hoekenga OA. The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil. 2005;274:175–195.
   Web of Science ®Google Scholar
• Kochian LV, Hoekenga OA, Piñeros MA. How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annual Rev Plant Biol. 2004;55:459–493.
   PubMed Web of Science ®Google Scholar
• Ma JF. Syndrome of aluminum toxicity and diversity of aluminum resistance in higher plants. Int Rev Cytol. 2007;264:225–252.
   PubMed Web of Science ®Google Scholar
• Kochian LV, Piñeros MA, Liu J, et al. Plant adaptation to acid soils: the molecular basis for crop aluminum resistance. Annu Rev Plant Biol. 2015;66:571–598.
   PubMed Web of Science ®Google Scholar
• Iuchi S, Koyama H, Iuchi A, et al. Zinc finger protein STOP1 is critical for proton tolerance in Arabidopsis and coregulates a key gene in aluminum tolerance. Proc Natl Acad Sci USA. 2007;104:9900–9905.
   PubMed Web of Science ®Google Scholar
• Yamaji N, Huang CF, Nagao S, et al. A zinc finger transcription factor ART1 regulates multiple genes implicated in aluminum tolerance in rice. Plant Cell. 2009;21:3339–3349.
   PubMed Web of Science ®Google Scholar
• Arenhart RA, Lima JC, Pedron M, et al. Involvement of ASR genes in aluminium tolerance mechanisms in rice. Plant Cell Environ. 2013;36:52–67.
   PubMed Web of Science ®Google Scholar
• Ding ZJ, Yan JY, Xu XY, et al. WRKY46 functions as a transcriptional repressor of ALMT1, regulating aluminum-induced malate secretion in Arabidopsis. Plant J. 2013;76:825–835.
   PubMed Web of Science ®Google Scholar
• Tokizawa M, Kobayashi Y, Saito T, et al. Sensitive to proton rhizotoxicity1, calmodulin binding transcription activator 2, and other transcription factors are involved in aluminum-activated malate transporter1 expression. Plant Physiol. 2015;167:991–1003.
   PubMed Web of Science ®Google Scholar
• Li GZ, Wang ZQ, Yokosho K, et al. Transcription factor WRKY22 promotes aluminum tolerance via activation of OsFRDL4 expression and enhancement of citrate secretion in rice (Oryza sativa). New Phytol. 2018;219:149–162.
   PubMed Web of Science ®Google Scholar
• Sawaki Y, Iuchi S, Kobayashi Y, et al. STOP1 regulates multiple genes that protect Arabidopsis from proton and aluminum toxicities. Plant Physiol. 2009;150:281–294.
   PubMed Web of Science ®Google Scholar
• Hoekenga OA, Maron LG, Piñeros MA, et al. AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. Proc Natl Acad Sci USA. 2006;103:9738–9743.
   PubMed Web of Science ®Google Scholar
• Liu J, Magalhaes JV, Shaff J, et al. Aluminum-activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminum tolerance. Plant J. 2009;57:389–399.
   PubMed Web of Science ®Google Scholar
• Huang CF, Yamaji N, Mitani N, et al. A bacterial-type ABC transporter is involved in aluminum tolerance in rice. Plant Cell. 2009;21:655–667.
   PubMed Web of Science ®Google Scholar
• Tsutsui T, Yamaji N, Ma JF. Identification of a cis-acting element of ART1, a C2H2-type zinc-finger transcription factor for aluminum tolerance in rice. Plant Physiol. 2011;156:925–931.
   PubMed Web of Science ®Google Scholar
• Huang S, Gao J, You J, et al. Identification of STOP1-like proteins associated with aluminum tolerance in sweet sorghum (Sorghum bicolor L.). Front Plant Sci. 2018;9:258.
   PubMed Web of Science ®Google Scholar
• Chen XY, Kim JY. Callose synthesis in higher plants. Plant Signal Behav. 2009;4:489–492.
   PubMedGoogle Scholar
• Horst WJ. uschel A-KP, Schmohl N. Induction of callose formation is a sensitive marker for genotypic aluminium sensitivity in maize. Plant Soil. 1997;192:23–30.
   Web of Science ®Google Scholar
• Yang ZM, Sivaguru M, Horst WJ, et al. Aluminium tolerance is achieved by exudation of citric acid from roots of soybean (Glycine max). Physiol Plant. 2000;110:72–77.
   Web of Science ®Google Scholar
• Hirano Y, Walthert L, Brunner I. Callose in root apices of European chestnut seedlings: A physiological indicator of aluminum stress. Tree Physiol. 2006;26:431–440.
   PubMed Web of Science ®Google Scholar
• Sivaguru M, Fujiwara T, Samaj J, et al. Aluminum-induced 1-3-beta-D-glucan inhibits cell-to-cell trafficking of molecules through plasmodesmata. A new mechanism of aluminum toxicity in plants. Plant Physiol. 2000;124:991–1005.
   PubMed Web of Science ®Google Scholar
• Sivaguru M, Horst WJ, Eticha D, et al. Aluminum inhibits apoplastic flow of high-molecular weight solutes in root apices of Zea mays L. J Plant Nutr Soil Sci. 2006;169:679–690.
   Web of Science ®Google Scholar
• Zavaliev R, Ueki S, Epel BL, et al. Biology of callose (beta-1,3-glucan) turnover at plasmodesmata. Protoplasma. 2011;248:117–130.
   PubMed Web of Science ®Google Scholar
• Cruz-Ortega R, Cushman JC, Ownby JD. cDNA clones encoding 1,3-beta- glucanase and a fimbrin-like cytoskeletal protein are induced by Al toxicity in wheat roots. Plant Physiol. 1997;114:1453–1460.
   PubMed Web of Science ®Google Scholar
• Goodwin SB, Sutter TR. Microarray analysis of Arabidopsis genome response to aluminum stress. Biologia Plantarum. 2009;53:85–99.
   Web of Science ®Google Scholar
• Tsutsui T, Yamaji N, Huang CF, et al. Comparative genome-wide transcriptional analysis of Al-responsive genes reveals novel Al tolerance mechanisms in rice. Plos one. 2012;7:e48197.
   PubMed Web of Science ®Google Scholar
• Zhang H, Shi WL, You JF, et al. Transgenic Arabidopsis thaliana plants expressing a beta-1,3-glucanase from sweet sorghum (Sorghum bicolor L.) show reduced callose deposition and increased tolerance to aluminium toxicity. Plant Cell Environ. 2015;38:1178–1188.
   PubMed Web of Science ®Google Scholar
• Ohyama Y, Ito H, Kobayashi Y, et al. Characterization of AtSTOP1 orthologous genes in tobacco and other plant species. Plant Physiol. 2013;162:1937–1946.
   PubMed Web of Science ®Google Scholar
• Fan W, Lou HQ, Gong YL, et al. Characterization of an inducible C2H2-type zinc finger transcription factor VuSTOP1 in rice bean (Vigna umbellata) reveals differential regulation between low pH and aluminum tolerance mechanisms. New Phytol. 2015;208:456–468.
   PubMed Web of Science ®Google Scholar
• Yang L, Mo W, Yu X, et al. Reconstituting Arabidopsis CRY2 signaling pathway in mammalian cells reveals regulation of transcription by direct binding of CRY2 to DNA. Cell Rep. 2018;24:585–593.e4.
   PubMed Web of Science ®Google Scholar
• Gao J, Wang X, Zhang M, et al. Trp triad-dependent rapid photoreduction is not required for the function of Arabidopsis CRY1. Proc Natl Acad Sci USA. 2015;112:9135–9140.
   PubMed Web of Science ®Google Scholar
• Liu H, Yu X, Li K, et al. Photoexcited CRY2 interacts with CIB1 to regulate transcription and floral initiation in Arabidopsis. Science. 2008;322:1535–1539.
   PubMed Web of Science ®Google Scholar
• Fang RX, Nagy F, Sivasubramaniam S, et al. Multiple cis regulatory elements for maximal expression of the cauliflower mosaic virus 35S promoter in transgenic plants. Plant Cell. 1989;1:141–150.
   PubMed Web of Science ®Google Scholar
• Li H, Wang J, Wang J, et al. Structural mechanism of DNA recognition by the p202 HINa domain: insights into the inhibition of Aim2-mediated inflammatory signalling. Acta Cryst F. 2014;70:21–29.
   Google Scholar
• Wang K, Gao Y, Peng X, et al. Using FAM labeled DNA oligos to do RNA electrophoretic mobility shift assay. Mol Biol Rep. 2010;37:2871–2875.
   PubMed Web of Science ®Google Scholar
• Li H, Wang ZX, Wu JW. Comparative purification and characterization of two HIN domains, hematopoietic interferon-inducible nuclear antigens with a 200-amino-acid repeat, in murine AIM2-like receptors. Biosci Biotechnol Biochem. 2013;77:2283–2287.
   PubMed Web of Science ®Google Scholar
• Qin X, Huang S, Liu Y, et al. Overexpression of A RING finger ubiquitin ligase gene AtATRF1 enhances aluminium tolerance in Arabidopsis thaliana. J Plant Biol. 2017;60:66–74.
   Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods. 2001;25:402–408.
   PubMed Web of Science ®Google Scholar
• Köhle H, Jeblick W, Poten F, et al. Chitosan-elicited callose synthesis in soybean cells as a Ca2+-dependent process. Plant Physiol. 1985;77:544–551.
   PubMed Web of Science ®Google Scholar
• Kobayashi Y, Ohyama Y, Kobayashi Y, et al. STOP2 activates transcription of several genes for Al- and low pH-tolerance that are regulated by STOP1 in Arabidopsis. Mol Plant. 2014;7:311–322.
   PubMed Web of Science ®Google Scholar
• Sawaki Y, Kobayashi Y, Kihara-Doi T, et al. Identification of a STOP1-like protein in Eucalyptus that regulates transcription of Al tolerance genes. Plant Sci. 2014;223:8–15.
   PubMed Web of Science ®Google Scholar
• Che J, Tsutsui T, Yokosho K, et al. Functional characterization of an aluminum (Al)-inducible transcription factor, ART2, revealed a different pathway for Al tolerance in rice. New Phytol. 2018;220:209–218.
   PubMed Web of Science ®Google Scholar
• Magalhaes JV, Liu J, Guimarães CT, et al. A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum. Nat Genet. 2007;39:1156–1161.
   PubMed Web of Science ®Google Scholar
• Daspute AA, Kobayashi Y, Panda SK, et al. Characterization of CcSTOP1; a C2H2-type transcription factor regulates Al tolerance gene in pigeonpea. Planta. 2018;247:201–214.
   PubMed Web of Science ®Google Scholar
• Zhang G, Hoddinott J, Taylor GJ. Characterization of 1,3-β-D-glucan (callose) synthesis in roots of Triticum aestivum in response to aluminum toxicity. J Plant Physiol. 1994;144:229–234.
   Web of Science ®Google Scholar
• Sivaguru M, Liu J, Kochian LV. Targeted expression of SbMATE in the root distal transition zone is responsible for sorghum aluminum resistance. Plant J. 2013;76:297–307.
   PubMed Web of Science ®Google Scholar
• Wissemeier AH, Horst WJ. Effect of calcium supply on aluminium-induced callose formation, its distribution and persistence in roots of soybean (Glycine max (L.)Merr.). J Plant Physiol. 1995;145:470–476.
   Web of Science ®Google Scholar
• Yang JL, Zhu XF, Peng YX, et al. Cell wall hemicellulose contributes significantly to aluminum adsorption and root growth in Arabidopsis. Plant Physiol. 2011;155:1885–1892.
   PubMed Web of Science ®Google Scholar
• Llugany M, Massot N, Wissemeier AH, et al. Aluminium tolerance of maize cultivars as assessed by callose production and root elongation. J Plant Nutr Soil Sci. 1994;157:447–451.
   Web of Science ®Google Scholar
• Maron LG, Kirst M, Mao C, et al. Transcriptional profiling of aluminum toxicity and tolerance responses in maize roots. New Phytol. 2008;179:116–128.
   PubMed Web of Science ®Google Scholar
• Yang JL, Li YY, Zhang YJ, et al. Cell wall polysaccharides are specifically involved in the exclusion of aluminum from the rice root apex. Plant Physiol. 2008;146:602–611.
   PubMed Web of Science ®Google Scholar