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Identification of the LEA family members from Caragana korshinskii (Fabaceae) and functional characterization of CkLEA2-3 in response to abiotic stress in Arabidopsis

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Abstract

Plants are exposed to different abiotic stresses that affect growth, development, and productivity. Previous studies have shown that late embryogenesis abundant (LEA) proteins play important roles in plant adaptation to abiotic stresses. However, reports that demonstrate their biological functions, especially in Caragana korshinskii Kom., are still very limited. In this study, 26 LEA genes were identified from dehydration-treated suppressive subtractive hybridizations cDNA library and transcriptome sequencing data of C. korshinskii, and were classified into seven groups according to their structural features. Quantitative real-time PCR analysis revealed that the CkLEAs were induced by abscisic acid (ABA) and diverse abiotic stresses and widely expressed in various tissues. Moreover, overexpression of CkLEA2-3 in Arabidopsis thaliana L. Heynh resulted in enhanced tolerance to ABA treatment, and osmotic and salt stresses during seed germination. CkLEA2-3 overexpression lines also exhibited resistance to drought stress during seedling development. Taken together, our results indicate that CkLEA2-3 plays positive roles in conferring abiotic stress tolerance in Arabidopsis.

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References

  • Baker J, Van Dennsteele C, Dure L (1988) Sequence and characterization of 6 Lea proteins and their genes from cotton. Plant Mol Biol 11:277–291

    Article  CAS  PubMed  Google Scholar 

  • Bies-Etheve N, Gaubier-Comella P, Debures A, Lasserre E, Jobet E, Raynal M, Cooke R, Delseny M (2008) Inventory, evolution and expression profiling diversity of the LEA (late embryogenesis abundant) protein gene family in Arabidopsis thaliana. Plant Mol Biol 67:107–124

    Article  CAS  PubMed  Google Scholar 

  • Boucher V, Buitink J, Lin X, Boudet J, Hoekstra FA, Hundertmark M, Renard D, Leprince O (2010) MtPM25 is an atypical hydrophobic late embryogenesis-abundant protein that dissociates cold and desiccation-aggregated proteins. Plant Cell Environ 33:418–430

    Article  CAS  PubMed  Google Scholar 

  • Campo S, Baldrich P, Messeguer J, Lalanne E, Coca M, San Segundo B (2014) Overexpression of a calcium-dependent protein kinase confers salt and drought tolerance in rice by preventing membrane lipid peroxidation. Plant Physiol 165:688–704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng J (2013) Spatial-temporal variability of Caragana korshinskii vegetation growth in the Loess Plateau. Sci Silvae Sin 49:14–20

    Google Scholar 

  • Choi DW, Close TJ (2000) A newly identified barley gene, Dhn12 encoding a YSK2 DHN, is located on chromosome 6H and has embryo-specific expression. Theor Appl Genet 100:1274–1278

    Article  CAS  Google Scholar 

  • Choudhury S, Panda P, Sahoo L, Panda SK (2013) Reactive oxygen species signaling in plants under abiotic stress. Plant Signal Behav 8:e23681

    Article  CAS  PubMed  Google Scholar 

  • Close TJ, Kortt AA, Chandler PM (1989) A cDNA-based comparison of dehydration-induced proteins (dehydrins) in barley and corn. Plant Mol Biol 13:95–108

    Article  CAS  PubMed  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Cuevas-Velazquez CL, Saab-Rincon G, Reyes JL, Covarrubias AA (2016) The unstructured N-terminal region of arabidopsis group 4 late embryogenesis abundant proteins (LEA) is required for folding and for chaperone-like activity under water deficit. J Biol Chem 291:10893–10903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • DaCosta M, Huang BR (2007) Changes in antioxidant enzyme activities and lipid peroxidation for bentgrass species in response to drought stress. J Am Soc Hortic Sci 132:319–326

    Article  CAS  Google Scholar 

  • Dure L, Greenway SC, Galau GA (1981) Developmental biochemistry of cottonseed embryogenesis and germination: changing messenger ribonucleic acid populations as shown by in vitro and in vivo protein synthesis. Biochemistry 20:4169–4178

    Article  PubMed  Google Scholar 

  • Dure L, Crouch M, Harada J, Ho TH, Mundy J, Quatrano R, Thomas T, Sung ZR (1989) Common amino acid sequence domains among the LEA proteins of higher plants. Plant Mol Biol 12:475–486

    Article  CAS  PubMed  Google Scholar 

  • Finkelstein RR (1993) Abscisic acid-insensitive mutations provide evidence for stage-specific signal pathways regulating expression of an Arabidopsis late embryogenesis-abundant (lea) gene. Mol Gen Genet 238:401–408

    Article  CAS  PubMed  Google Scholar 

  • Finkelstein RR, Rock CD (2013) Abscisic acid synthesis and response. Arabidopsis Book 11:e0166

    Article  PubMed  PubMed Central  Google Scholar 

  • Finkelstein RR, Gampala SSL, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14:S15–S45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finn RD, Mistry J, Tate J et al (2010) The Pfam protein families database. Nucl Acids Res 38:D211–D222

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Souriau N, Perret S, Lelandais M, Kunert KJ, Pruvost C, Jouanin L (1995) Overexpression of glutathione reductase but not glutathione synthetase leads to increases in antioxidant capacity and resistance to photoinhibition in poplar trees. Plant Physiol 109:1047–1057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsing YC, Chen ZY, Shih MD, Hsieh JS, Chow TY (1995) Unusual sequences of group 3 LEA mRNA inducible by maturation or drying in soybean seeds. Plant Mol Biol 29:863–868

    Article  CAS  PubMed  Google Scholar 

  • Huang LP, Jia J, Zhao XX, Zhang MY, Huang XX, Ji E et al (2018) The ascorbate peroxidase APX1 is a direct target of a zinc finger transcription factor ZFP36 and a late embryogenesis abundant protein OsLEA5 interacts with ZFP36 to co-regulate OsAPX1 in seed germination in rice. Biochem Biophys Res Commun 495:339–345

    Article  CAS  PubMed  Google Scholar 

  • Hundertmark M, Hincha DK (2008) LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genom 9:118

    Article  CAS  Google Scholar 

  • Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 47:377–403

    Article  CAS  PubMed  Google Scholar 

  • Jaspard E, Macherel D, Hunault G (2012) Computational and statistical analyses of amino acid usage and physico-chemical properties of the twelve late embryogenesis abundant protein classes. PLoS One 7:e36968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ji XM, Dong BD, Shiran B et al (2011) Control of abscisic acid catabolism and abscisic acid homeostasis Iis important for reproductive stage stress tolerance in cereals. Plant Physiol 156:647–662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jia FJ, Qi SD, Li H, Liu P, Li PC, Wu CG, Zheng CC, Huang JG (2014) Overexpression of Late Embryogenesis Abundant 14 enhances Arabidopsis salt stress tolerance. Biochem Biophys Res Commun 454:505–511

    Article  CAS  PubMed  Google Scholar 

  • Kovacs D, Kalmar E, Torok Z, Tompa P (2008) Chaperone activity of ERD10 and ERD14, two disordered stress-related plant proteins. Plant Physiol 147:381–390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lan T, Gao J, Zeng QY (2013) Genome-wide analysis of the LEA (late embryogenesis abundant) protein gene family in Populus trichocarpa. Tree Genet Genomes 9:253–264

    Article  Google Scholar 

  • Leung J, Giraudat J (1998) Abscisic acid signal transduction. Annu Rev Plant Physiol Plant Mol Biol 49:199–222

    Article  CAS  PubMed  Google Scholar 

  • Li YZ, Jia FJ, Yu YL, Luo L, Huang LG, Yang GD et al (2014) The SCF E3 ligase AtPP2-B11 plays a negative role in response to drought stress in Arabidopsis. Plant Mol Biol Rep 32:943–956

    Article  CAS  Google Scholar 

  • Li SF, Fan CM, Li Y et al (2016) Effects of drought and salt-stresses on gene expression in Caragana korshinskii seedlings revealed by RNA-seq. BMC Genom 17:200

    Article  CAS  Google Scholar 

  • Lim CW, Lim S, Baek W, Lee SC (2014) The pepper late embryogenesis abundant protein CaLEA1 acts in regulating abscisic acid signaling, drought and salt stress response. Physiol Plant 154:526–542

    Article  CAS  PubMed  Google Scholar 

  • Liu DY, Liu XC, Du F, Wang HX, Wen B, Zhu WW, Xu YY (2010) Effect of salt stress on germination of Caragana korshinskii Kom and Medicago sativa L. seed. Seed 29:79–84

    Google Scholar 

  • Liu H, Yu C, Li H, Ouyang B, Wang T, Zhang J, Wang X, Ye Z et al (2015) Overexpression of ShDHN, a dehydrin gene from Solanum habrochaites enhances tolerance to multiple abiotic stresses in tomato. Plant Sci 231:198–211

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)). Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Long Y, Wang YY, Wu SS, Wang J, Tian XJ, Pei XW (2015) De novo assembly of transcriptome sequencing in Caragana korshinskii Kom. and characterization of EST-SSR markers. PLoS One 10:e0115805

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manfre AJ, Lanni LM, Marcotte WR Jr (2006) The Arabidopsis group 1 late embryogenesis abundant protein ATEM6 is required for normal seed development. Plant Physiol 140:140–149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niu X (1998) Biological characters of cultivars in Caragana. Acta Agric Boreali Sin 13:123–130

    Google Scholar 

  • Olvera-Carrillo Y, Campos F, Reyes JL, Garciarrubio A, Covarrubias AA (2010) Functional analysis of the group 4 late embryogenesis abundant proteins reveals their relevance in the adaptive response during water deficit in Arabidopsis. Plant Physiol 154:373–390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma A, Kumar D, Kumar S, Rampuria S, Reddy AR, Kirti PB (2016) Ectopic expression of an atypical hydrophobic group 5 LEA protein from wild peanut, Arachis diogoi confers abiotic stress tolerance in tobacco. PLoS One 11:e0150609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shih MD, Hoekstra FA, Hsing YIC (2008) Late embryogenesis abundant proteins. Adv Bot Res 48:211–255

    Article  CAS  Google Scholar 

  • Sivamani E, Bahieldin A, Wraith JM, Al-Niemi T, Dyer WE, Ho TD, Qu R (2000) Improved biomass productivity and water use efficiency under water deficit conditions in transgenic wheat constitutively expressing the barley HVA1 gene. Plant Sci 155:1–9

    Article  CAS  PubMed  Google Scholar 

  • Sun XL, Rikkerink EHA, Jones WT, Uversky VN (2013) Multifarious roles of intrinsic disorder in proteins illustrate its broad impact on plant biology. Plant Cell 25:38–55

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599

    Article  CAS  PubMed  Google Scholar 

  • Tunnacliffe A, Wise MJ (2007) The continuing conundrum of the LEA proteins. Naturwissenschaften 94:791–812

    Article  CAS  PubMed  Google Scholar 

  • Wang XS, Zhu HB, Jin GL, Liu HL, Wu WR, Zhu J (2007) Genome-scale identification and analysis of LEA genes in rice (Oryza sativa L.). Plant Sci 172:414–420

    Article  CAS  Google Scholar 

  • Wang M, Li P, Li C et al (2014) SiLEA14, a novel atypical LEA protein, confers abiotic stress resistance in foxtail millet. BMC Plant Biol 14:290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wellburn AM, Creissen GP, Lake JA, Mullineaux PM, Wellburn AR (1998) Tolerance to atmospheric ozone in transgenic tobacco over-expressing glutathione synthetase in plastids. Physiol Plant 104:623–629

    Article  CAS  Google Scholar 

  • Xiao SC, Xiao HL, Peng XM, Wang WP, Chen XH, Tian QY (2015) Dendroecological assessment of Korshinsk peashrub (Caragana korshinskii Kom.) from the perspective of interactions among growth, climate, and topography in the western Loess Plateau, China. Dendrochronologia 33:61–68

    Article  Google Scholar 

  • Xie C, Zhang R, Qu Y et al (2012) Overexpression of MtCAS31 enhances drought tolerance in transgenic Arabidopsis by reducing stomatal density. New Phytol 195:124–135

    Article  CAS  PubMed  Google Scholar 

  • Xu DH, Fang XW, Su PX, Wang G (2012) Ecophysiological responses of Caragana korshinskii Kom. under extreme drought stress: leaf abscission and stem survives. Photosynthetica 50:541–548

    Article  CAS  Google Scholar 

  • Yang Q, Zhang T, Wang Y et al (2013) Construction of a suppression subtractive hybridization library of Caragana korshinskii under drought stress and cloning of CkWRKY1 gene. Sci Silvae Sin 49:62–68

    CAS  Google Scholar 

  • Yang Q, Yin JJ, Li G, Qi LW, Yang FY, Wang RG, Li GJ (2014) Reference gene selection for qRT-PCR in Caragana korshinskii Kom. under different stress conditions. Mol Biol Rep 41:2325–2334

    Article  CAS  PubMed  Google Scholar 

  • Yu J, Lai Y, Wu X, Wu G, Guo C (2016) Overexpression of OsEm1 encoding a group I LEA protein confers enhanced drought tolerance in rice. Biochem Biophys Res Commun 478:703–709

    Article  CAS  PubMed  Google Scholar 

  • Zamora-Briseno JA, de Jimenez ES (2016) A LEA 4 protein up-regulated by ABA is involved in drought response in maize roots. Mol Biol Rep 43:221–228

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Lu S, Jiang C, Wang Y, Lv B, Shen J et al (2014) RcLEA, a late embryogenesis abundant protein gene isolated from Rosa chinensis, confers tolerance to Escherichia coli and Arabidopsis thaliana and stabilizes enzyme activity under diverse stresses. Plant Mol Biol 85:333–347

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We deeply appreciated Dr. Mark Goettel, Editor-in-Chief of Biocontrol Science & Technology, for polishing the manuscript carefully. This work was supported by the grants from National Natural Science Foundation of China (31560199) to Qi Yang.

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GL and XY conceived and designed the experiments. XY, WY, QY, and YZ carried out the experiments. XY and GL drafted the manuscript. QY, XH, FY, and RW participated in the design of experiments and edited the manuscript. All authors read, edited, and approved the manuscript.

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Correspondence to Guojing Li.

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Supplementary material 1 (DOC 112 kb)

40415_2019_529_MOESM2_ESM.tif

Supplementary Fig. 1 qRT-PCR analysis of CkLEA2-3 expression level in leaves of overexpression lines. The T3 transgenic plants growing under normal condition were detected by quantitative real-time PCR. Expression values were calculated using 2−ΔCT method, and AtEF1α was used as an internal control. Means ± SEs, n = 3 (TIFF 265 kb)

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Yu, X., Yue, W., Yang, Q. et al. Identification of the LEA family members from Caragana korshinskii (Fabaceae) and functional characterization of CkLEA2-3 in response to abiotic stress in Arabidopsis. Braz. J. Bot 42, 227–238 (2019). https://doi.org/10.1007/s40415-019-00529-y

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