Abstract
Jacalin-related lectins (JRLs) are carbohydrate-binding proteins widely present in plants and have one or more jacalin domains in common. However, JRLs’ structural types and functions are still poorly understood. In the present study, a total of 67 wheat (Triticum aestivum) JRL genes were identified through an exhausted search of EST database coupling with genome walking using published 454 sequence reads of Chinese Spring. A comparison of the translated wheat JRL proteins with those from other plants showed plant JRLs generally had low sequence similarity within and between species but exhibited conserved modular domain structures. More JRL genes encoded multiple jacalin domains in Arabidopsis thaliana, whereas more genes encoded chimeric JRLs in cereal plants. Dirigent domain-containing JRL genes were Poaceae-specific and accounted for nearly half of the identified wheat JRL genes. The dirigent domains were evolutionarily significantly correlated with the covalently linked jacalin domains. A phylogenetic analysis showed JRL proteins have experienced a substantial diversification after speciation. Moreover, new structural features conserved across the taxa were identified. Digital expression analysis and RT-PCR assays showed the expression of wheat JRL genes was largely tissue specific, typically low, and mostly inducible by biotic and abiotic stresses and stress hormones. These results suggest plant JRLs are critical for plant adaptation to stressful environments.
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Abebe T, Skadsen RW, Kaeppler HF (2005) A proximal upstream sequence controls tissue-specific expression of Lem2, a salicylate-inducible barley lectin-like gene. Planta 221:170–183
Blanchard DJ, Cicek M, Chen J, Esen A (2001) Identification of beta-glucosidase aggregating factor (BGAF) and mapping of BGAF binding regions on Maize beta-glucosidase. J Biol Chem 276:11895–11901
Bourne Y, Zamboni V, Barre A, Peumans WJ, Van Damme EJM, Rougé P (1999) Helianthus tuberosus lectin reveals a widespread scaffold for mannose-binding lectins. Structure 7:1473–1482
Brenchley R, Spannagl M, Pfeiffer M, Barker GLA, D’Amore R, Allen AM, McKenzie N, Kramer M, Kerhornou A, Bolser DKS, Waite D, Trick M, Bancroft I, Gu Y, Huo N, Luo MC, Sehgal S, Gill B, Kianian S, Anderson O, Kersey P, Dvorak J, McCombie WR, Hall A, Mayer MFX, Hall N, Edwards KJ, Bevan MW, Hall N (2012) Analysis of the bread wheat genome using whole-genome shotgun sequencing. Nature 491:705–710
Bunn-Moreno MM, Campos-Neto A (1981) Lectin(s) extracted from seeds of Artocarpus integrifolia (jackfruit): potent and selective stimulator(s) of distinct human T and B cell function. J Immunol 127:427–429
Burow M, Losansky A, Muller R, Plock A, Kliebenstein DJ, Wittstock U (2009) The genetic basis of constitutive and herbivore-induced ESP-independent nitrile formation in Arabidopsis. Plant Physiol 149:561–574
Chang WC, Liu KL, Hsu FC, Jeng ST, Cheng YS (2012) Ipomoelin, a Jacalin-related lectin with a compact tetrameric association and versatile carbohydrate binding properties regulated by its N terminus. PLoS ONE 7:e40618. doi:10.1371/journal.pone.0040618
Chaw SM, Chang CC, Chen HL, Li WH (2004) Dating the monocot–dicot divergence and the origin of core eudicots using whole chloroplast genomes. J Mol Evol 58:424–441
Chisholm ST, Mahajan SK, Whitman SA, Yamamoto ML, Carrington JC (2000) Cloning of the Arabidopsis RTM1 gene, which controls restriction of long-distance movement of tobacco etch virus. Proc Natl Acad Sci USA 97:489–494
Claes B, Dekeyser R, Villarroel R, Van den Bulcke M, Bauw G, Van Montagu M, Caplan A (1990) Characterization of a rice gene showing organ-specific expression in response to salt stress and drought. Plant Cell 2:19–27
De Souza Filho GA, Ferreira BS, Dias JM, Queiroz KS, Branco AT, Bressan-smith RE, Oliveira JG, Garcia AB (2003) Accumulation of SALT protein in rice plants as a response to environmental stress. Plant Sci 164:623–628
Fisher LD, van Belle G (1993) Biostatistics: a methodology for the health sciences. In: Fisher LD, van Belle G (eds). Wiley, New York, pp xxii + 991
Gallego del Sol F, Nagano C, Cavada BS, Calvete JJ (2005) The first crystal structure of a Mimosoideae lectin reveals a novel quaternary arrangement of a widespread domain. J Mol Biol 353:574–583
Garcia AB, Engler JA, Claes B, Villarroel R, Van Montagu M, Gerats T, Caplan A (1998) The expression of the salt-responsive gene salT from rice is regulated by hormonal and developmental cues. Planta 207:172–180
Goh CS, Bogan AA, Joachimiak M, Walther D, Cohen FE (2000) Co-evolution of proteins with their interaction partners. J Mol Biol 299:283–293
Huang X, Madan A (1999) CAP3: a DNA sequence assembly program. Genome Res 9:868–877
Imanishi S, Kito-Nakamura K, Matsuoka K, Morikami A, Nakamura K (1997) A major jasmonate-inducible protein of sweet potato, ipomoelin, is an ABA-independent wound-inducible protein. Plant Cell Physiol 38:643–652
Jiang JF, Han Y, Xing LJ, Xu YY, Xu ZH, Chong K (2006) Cloning and expression of a novel cDNA encoding a mannose-specific jacalin-related lectin from Oryza sativa. Toxicon 47:133–139
Jiang SY, Ma ZG, Ramachandran S (2010) Evolutionary history and stress regulation of the lectin superfamily in higher plants. BMC Evol Biol 10:79
Kellogg EA (2001) Evolutionary history of the grasses. Plant Physiol 125:1198–1205
Kim ST, Cho KS, Yu S, Kim SG, Hong JC, Han CD, Bae DW, Nam MH, Kang KY (2003) Proteomic analysis of differentially expressed proteins induced by rice blast fungus and elicitor in suspension-cultured rice cells. Proteomics 3:2368–2378
Kittur FS, Yu HY, Bevan DR, Esen A (2010) Deletion of the N-terminal dirigent domain in maize β-glucosidase aggregating factor and its homolog sorghum lectin dramatically alters the sugar-specificities of their lectin domains. Plant Physiol Biochem 48:731–734
Letunic I, Copley RR, Schmidt S, Ciccarelli FD, Doerks T, Schultz J, Ponting CP, Bork P (2004) SMART 4.0: towards genomic data integration. Nucleic Acids Res 32:D142–D144
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408
Ma QH, Tian B, Li YL (2010) Overexpression of a wheat jasmonate-regulated lectin increases pathogen resistance. Biochimie 92:187–193
Ma QH, Zhen WB, Liu YC (2013) Jacalin domain in wheat jasmonate-regulated protein Ta-JA1 confers agglutinating activity and pathogen resistance. Biochimie 95:359–365
Meagher JL, Winter HC, Ezell P, Goldstein IJ, Stuckey JA (2005) Crystal structure of banana lectin reveals a novel second sugar binding site. Glycobiology 15:1033–1042
Nagano AJ, Fukao Y, Fujiwara M, Nishimura M, Hara-Nishimura I (2008) Antagonistic jacalin-related lectins regulate the size of ER body-type β-glucosidase complexes in Arabidopsis thaliana. Plant Cell Physiol 49:969–980
Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140:411–432
Qin QM, Zhang Q, Zhao WS, Wang YY, Peng YL (2003) Identification of a lectin gene induced in rice in response to Magnaporthe grisea infection. Acta Botanica Sinica 45:76–81
Raval S, Gowda SB, Singh DD, Chandra NR (2004) A database analysis of jacalin-like lectins: sequence-structure-function relationships. Glycobiology 14:1247–1263
Richly E, Kurth J, Leister D (2002) Mode of amplification and reorganization of resistance genes during recent Arabidopsis thaliana evolution. Mol Biol Evol 19:76–84
Schultz J, Milpetz F, Bork P, Ponting CP (1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci USA 95:5857–5864
Subramanyam S, Sardesai N, Puthoff DP, Meyer JM, Nemacheck JA, Gonzalo M, Williams CE (2006) Expression of two wheat defense-response genes, Hfr-1 and Wci-1, under biotic and abiotic stresses. Plant Sci 170:90–103
Subramanyam S, Smith DF, Clemens JC, Webb MA, Sardesai N, Williams CE (2008) Functional characterization of HFR-1, a high mannose N-glycan-specific wheat lectin induced by Hessian fly larvae. Plant Physiol 147:1412–1426
Swigonová Z, Lai J, Ma J, Ramakrishna W, Llaca V, Bennetzen JL, Messing J (2004) Close split of sorghum and maize genome progenitors. Genome Res 14:1916–1923
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Van Damme EJ, Peumans WJ, Barre A, Rougé P (1998) Plant lectins: a composite of several distinct families of structurally and evolutionary related proteins with diverse biological roles. Crit Rev Plant Sci 17:575–692
Van Damme EJ, Lannoo N, Peumans WJ (2008) Plant lectins. Adv Bot Res 48:107–209
von Koskull-Döring PV, Scharf KD, Nover L (2007) The diversity of plant heat stress transcription factor. Trends Plant Sci 20:452–457
Wang XM, Ma QH (2005) Characterization of a jasmonate-regulated wheat protein related to a beta-glucosidase-aggregating factor. Plant Physiol Biochem 43:185–192
Wang X, Shi X, Hao B, Ge S, Luo J (2005) Duplication and DNA segmental loss in the rice genome: implications for diploidization. New Phytol 165:937–946
Williams CE, Collier CC, Nemacheck JA, Liang C, Cambron SE (2002) A lectin-like wheat gene responds systemically to attempted feeding by avirulent first-instar Hessian fly larvae. J Chem Ecol 28:1411–1428
Xiang Y, Song M, Wei ZY, Tong J, Zhang LX, Xiao L, Ma ZQ, Wang Y (2011) A jacalin-related lectin-like gene in wheat is a component of the plant defence system. J Exp Bot 62:5471–5483
Xiao S, Emerson B, Ratanasut K, Patrick E, O’Neill C, Bancroft I, Turner JG (2004) Origin and maintenance of a broad-spectrum disease resistance locus in Arabidopsis. Mol Biol Evol 21:1661–1672
Yamaji Y, Maejima K, Komatsu K, Shiraishi T, Okano Y, Himeno M, Sugawara K, Neriya Y, Minato N, Miura C, Hashimoto M, Namba S (2012) Lectin-mediated resistance impairs plant virus infection at the cellular level. Plant Cell 24:778–793
Yao GQ, Zhang JL, Yang LL, Xu HB, Jiang YM, Xiong L, Zhang CQ, Zhang ZZ, Ma ZQ, Sorrells ME (2007) Genetic mapping of two powdery mildew resistance genes in einkorn (Triticum monococcum L.) accessions. Theor Appl Genet 114:351–358
Yong WD, Xu YY, Xu WZ, Wang X, Li N, Wu JS, Liang TB, Chong K, Xu ZH, Tan KH, Zhu ZQ (2003) Vernalization induced flowering in wheat is mediated by a lectin-like gene VER2. Planta 217:261–270
Zhang Y, Wang L (2005) The WRKY transcription factor superfamily: its origin in eukaryotes and expansion in plants. BMC Evol Biol 5:1–12
Zhang W, Peumans WJ, Barre A, Astoul CH, Rovira P, Rougé P, Proost P, Truffa-Bachi P, Jalali AA, Van Damme EJM (2000) Isolation and characterization of a jacalin-related mannose-binding lectin from salt-stressed rice (Oryza sativa) plants. Planta 210:970–978
Acknowledgments
This work was partially supported by NSFC program (30130054, 30025030), ‘973’ program (2010CB125900), Fundamental research Funds for the Central Universities (KYZ201202-4), and 111 project of Ministry of Education (grant no. Bo8025). Xiang Yang was partially supported by a fund from Engineering Technology Research Center of Guizhou Province (No. 20124006). The authors are grateful to the three anonymous reviewers for valuable comments and suggestions.
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Min Song and Wenqi Xu contributed equally to this paper.
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Online Resource 4. JRL genes and JRL structural domains of sorghum, rice, maize, B. distachyon, and A. thaliana (PDF 120 kb)
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Online Resource 6. Expression profiles of a selected set of TaJRL genes in Wangshuibai, as revealed by sqPCR (PDF 194 kb)
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Song, M., Xu, W., Xiang, Y. et al. Association of jacalin-related lectins with wheat responses to stresses revealed by transcriptional profiling. Plant Mol Biol 84, 95–110 (2014). https://doi.org/10.1007/s11103-013-0121-5
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DOI: https://doi.org/10.1007/s11103-013-0121-5