Abstract
Recent discoveries showed that hybrid proline rich type proteins were involved in plant responses to several environmental stresses. However, little is known about their roles in plant alkali stress adaptation, especially in wild soybean. Here, we isolated and characterized GsEARLI17, a novel the hybrid proline-rich protein type EARLI family gene from Glycine soja. Bioinformatic analysis showed that GsEARLI17 protein contained a conserved N-terminus hybrid proline-rich domain in and a C-terminus 8CM domain. Transcript abundance of GsEARLI17 was higher in young tissues than that in old tissues, and induced following exposure to salt and alkali treatments. GsEARLI17 overexpression in Arabidopsis influenced cuticles formation, as evidenced by thicker cuticles of transgenic lines, and enhanced plant tolerance to salt stress. Further observation was found that compared to the wild type Arabidopsis, overexpression of GsEARLI17 in Arabidopsis improved seed germination with higher leaf opening and greening rate during the early stages under alkali stress. GsEARLI17 exhibited enhanced alkaline tolerance with higher chlorophyll content, and lower malondialdehyde content at the adult developmental stage, and the expression levels of some alkali stress response marker genes NADP-ME, H + Ppase were higher in the GsEARLI17 overexpression lines than in wild-type plants. Taken together we suggest that GsEARLI17 reveal a positive role in enhancing plant tolerance of alkali stress in Arabidopsis.
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Arondel V, Vergnolle C, Cantrel C, Kader J-C (2000) Lipid transfer proteins are encoded by a small multigene family in Arabidopsis thaliana. Plant Sci 157:1–12
Battaglia M, Solorzano RM, Hernandez M, Cuellar-Ortiz S, Garcia-Gomez B, Marquez J, Covarrubias AA (2007) Proline-rich cell wall proteins accumulate in growing regions and phloem tissue in response to water deficit in common bean seedlings. Planta 225:1121–1133
Blanco-Portales R, Lopez-Raez JA, Bellido ML, Moyano E, Dorado G, Gonzalez-Reyes JA, Caballero JL, Munoz-Blanco J (2004) A strawberry fruit-specific and ripening-related gene codes for a HyPRP protein involved in polyphenol anchoring. Plant Mol Biol 55:763–780
Bradley DJ, Kjellbom P, Lamb CJ (1992) Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: a novel, rapid defense response. Cell 70:21–30.
Bubier J, Schlappi M (2004) Cold induction of EARLI1, a putative Arabidopsis lipid transfer protein, is light and calcium dependent. Plant Cell Environ 27:929–936
Chae L, Sudat S, Dudoit S, Zhu T, Luan S (2009) Diverse transcriptional programs associated with environmental stress and hormones in the Arabidopsis receptor-like kinase gene family. Mol Plant 2:84–107
Clark R, Zeto S (1996) Mineral acquisition by mycorrhizal maize grown on acid and alkaline soil. Soil Biol Biochem 28:1495–1503
Cushman JC, Meyer G, Michalowski CB, Schmitt JM, Bohnert HJ (1989) Salt stress leads to differential expression of two isogenes of phosphoenolpyruvate carboxylase during Crassulacean acid metabolism induction in the common ice plant. Plant cell 1
Dvorakova L, Cvrckova F, Fischer L (2007) Analysis of the hybrid proline-rich protein families from seven plant species suggests rapid diversification of their sequences and expression patterns. BMC genomics 8
Fahnenstich H, Saigo M, Niessen M, Zanor MI, Andreo CS, Fernie AR, Drincovich MF, Fluegge U-I, Maurino VG (2007) Alteration of organic acid metabolism in Arabidopsis overexpressing the maize C(4)NADP-malic enzyme causes accelerated senescence during extended darkness. Plant Physiol 145:640–652
Finkelstein RR (2010) The role of hormones during seed development and germination. Plant Hormones 549–573
Frelin C, Vigne P, Ladoux A, Lazdunski M (1988) The regulation of the intracellular pH in cells from vertebrates. Eur J Biochem 174:3–14
Fushimi T, Umeda M, Shimazaki T, Kato A, Toriyama K, Uchimiya H (1994) Nucleotide sequence of a rice cDNA similar to a maize NADP-dependent malic enzyme. Plant Mol Biol 24:965–967
Ge Y, Li Y, Zhu Y-M, Bai X, Lv D-K, Guo D, Ji W, Cai H (2010) Global transcriptome profiling of wild soybean (Glycine soja) roots under NaHCO3 treatment. BMC Plant Biol 10:153
Jang CS, Lee HJ, Chang SJ, Seo YW (2004) Expression and promoter analysis of the TaLTP1 gene induced by drought and salt stress in wheat (Triticum aestivum L.). Plant Sci 167:995–1001
José-Estanyol M, Gomis-Rüth FX, Puigdomènech P (2004) The eight-cysteine motif, a versatile structure in plant proteins. Plant Physiol Biochem 42:355–365
Larkin M, Blackshields G, Brown N, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948
Lee SB, Jung SJ, Go YS, Kim HU, Kim JK, Cho HJ, Park OK, Suh MC (2009) Two Arabidopsis 3-ketoacyl CoA synthase genes, KCS20 and KCS2/DAISY, are functionally redundant in cuticular wax and root suberin biosynthesis, but differentially controlled by osmotic stress. Plant J 60:462–475
Li R, Shi F, Fukuda K, Yang Y (2010) Effects of salt and alkali stresses on germination, growth, photosynthesis and ion accumulation in alfalfa (Medicago sativa L.). Soil Sci Plant Nutr 56:725–733
Lolle SJ, Berlyn GP, Engstrom EM, Krolikowski KA, Reiter W-D, Pruitt RE (1997) Developmental regulation of cell interactions in the Arabidopsis fiddlehead-1 mutant: a role for the epidermal cell wall and cuticle. Dev Biol 189:311–321
Molina A, García-Olmedo F (1997) Enhanced tolerance to bacterial pathogens caused by the transgenic expression of barley lipid transfer protein LTP2. Plant J 12:669–675
Nounjan N, Nghia PT, Theerakulpisut P (2012) Exogenous proline and trehalose promote recovery of rice seedlings from salt-stress and differentially modulate antioxidant enzymes and expression of related genes. J Plant Physiol 169:596–604
Pennell R (1998) Cell walls: structures and signals. Curr Opin Plant Biol 1:504–510
Somerville C, Bauer S, Brininstool G, Facette M, Hamann T, Milne J, Osborne E, Paredez A, Persson S, Raab T, Vorwerk S, Youngs H (2004) Toward a systems approach to understanding plant-cell walls. Science 306:2206–2211
Song S, Dai X, Zhang W-H (2012) A rice F-box gene, OsFbx352, is involved in glucose-delayed seed germination in rice. J Exp Bot 63:5559–5568
Takahashi M, Nakanishi H, Kawasaki S, Nishizawa NK, Mori S (2001) Enhanced tolerance of rice to low iron availability in alkaline soils using barley nicotianamine aminotransferase genes. Nat Biotechnol 19:466–469
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Thoma S, Kaneko Y, Somerville C (1993) A non-specific lipid transfer protein from Arabidopsis is a cell wall protein. Plant J 3:427–436
Wang H, Datla R, Georges F, Loewen M, Cutler AJ (1995) Promoters from kin1 and cor6.6, two homologous Arabidopsis thaliana genes: transcriptional regulation and gene expression induced by low temperature, ABA, osmoticum and dehydration. Plant Mol Biol 28:605–617
Wilkosz R, Schlappi M (2000) A gene expression screen identifies EARLI1 as a novel vernalization-responsive gene in Arabidopsis thaliana. Plant Mol Biol 44:777–787
Xu D, Huang X, Xu ZQ, Schlappi M (2011) The HyPRP gene EARLI1 has an auxiliary role for germinability and early seedling development under low temperature and salt stress conditions in Arabidopsis thaliana. Planta 234:565–577
Yamaguchi-Shinozaki K, Shinozaki K (1993a) Arabidopsis DNA encoding two desiccation-responsive rd29 genes. Plant Physiol 101:1119–1120
Yamaguchi-Shinozaki K, Shinozaki K (1993b) The plant hormone abscisic acid mediates the drought-induced expression but not the seed-specific expression of rd22, a gene responsive to dehydration stress in Arabidopsis thaliana. Mol Gen Genet 238:17–25
Yang C, Chong J, Li C, Kim C, Shi D, Wang D (2007) Osmotic adjustment and ion balance traits of an alkali resistant halophyte Kochia sieversiana during adaptation to salt and alkali conditions. Plant Soil 294:263–276
Yang C, Jianaer A, Li C, Shi D, Wang D (2008a) Comparison of the effects of salt-stress and alkali-stress on photosynthesis and energy storage of an alkali-resistant halophyte Chloris virgata. Photosynthetica 46:273–278
Yang C, Shi D, Wang D (2008b) Comparative effects of salt and alkali stresses on growth, osmotic adjustment and ionic balance of an alkali-resistant halophyte Suaeda glauca (Bge.). Plant Growth Regul 56:179–190
Yeats TH, Rose JK (2008) The biochemistry and biology of extracellular plant lipid-transfer proteins (LTPs). Protein Sci 17:191–198
Yelle S, Beeson RC, Trudel MJ, Gosselin A (1989) Acclimation of two tomato species to high atmospheric CO(2): II. ribulose-1,5-bisphosphate carboxylase/oxygenase and phosphoenolpyruvate carboxylase. Plant Physiol 90
Zhang Y, Schlappi M (2007) Cold responsive EARLI1 type HyPRPs improve freezing survival of yeast cells and form higher order complexes in plants. Planta 227:233–243
Zhang Y, Xu W, Li Z, Deng XW, Wu W, Xue Y (2008a) F-box protein DOR functions as a novel inhibitory factor for abscisic acid-induced stomatal closure under drought stress in Arabidopsis. Plant Physiol 148:2121–2133
Zhang Y-y, Li Y, Gao T, Zhu H, Wang D-j, Zhang H-w, Ning Y-s, Liu L-j, Wu Y-r, Chu C-c (2008b) Arabidopsis SDIR1 enhances drought tolerance in crop plants. Biosci Biotechnol Biochem 72:2251–2254
Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445
Acknowledgments
This work was supported by the National Natural Science Foundation of China (31171578), Heilongjiang Provincial Higher School Science and Technology Innovation Team Building Program (2011TD005), National basic scientific talent training fund projects (J1210069), and Ministry of Agriculture transgenic major projects (2011ZX08004).
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Liu, A., Yu, Y., Li, R. et al. A novel hybrid proline-rich type gene GsEARLI17 from Glycine soja participated in leaf cuticle synthesis and plant tolerance to salt and alkali stresses. Plant Cell Tiss Organ Cult 121, 633–646 (2015). https://doi.org/10.1007/s11240-015-0734-2
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DOI: https://doi.org/10.1007/s11240-015-0734-2