Skip to main content
SpringerLink
Log in

Overexpression of SbAP37 in rice alleviates concurrent imposition of combination stresses and modulates different sets of leaf protein profiles

  • Research Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

SbAP37 transcription factor contributes to a combination of abiotic stresses when applied simultaneously in rice. It modulates a plethora of proteins that might regulate the downstream pathways to impart salt stress tolerance.

Abstract

APETALA type of transcription factor was isolated from Sorghum bicolor (SbAP37), overexpressed in rice using a salt inducible abscisic acid 2 (ABA2) promoter through Agrobacterium tumefaciens following in planta method. Transgenics were confirmed by PCR amplification of SbAP37, hygromycin phosphotransferase (hptII) marker and ABA2 promoter and DNA blot analysis. Plants were exposed to 150 mM NaCl coupled with high day/night 36 ± 2/25 ± 2 °C temperatures and also drought stress by withholding water for 1-week separately at the booting stage. SbAP37 expression was 2.8- to 4.7-folds higher in transgenic leaf under salt, but 1.8- to 3.3-folds higher in roots under drought stress. Native gene expression analysis showed that it is expressed more in stem than in roots and leaves under 150 mM NaCl and 6% PEG stress. In the present study, proteomic analysis of transgenics exposed to 150 mM NaCl coupled with elevated temperatures was taken up using quadrupole time-of-flight (Q-TOF) mass spectrometry (MS). The leaf proteome revealed 11 down regulated, 26 upregulated, 101 common (shared), 193 newly synthesized proteins in transgenics besides 368 proteins in untransformed plants. Some of these protein sets appeared different and unique to combined stresses. Our results suggest that the SbAP37 has the potential to improve combined stress tolerance without causing undesirable phenotypic characters when used under the influence of ABA2 promoter.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

References

  • Agrawal GK, Yamazaki M, Kobayashi M, Hirochika R, Miyao A, Hirochika H (2001) Screening of the rice viviparous mutants generated by endogenous retrotransposon Tos17 insertion. Tagging of a zeaxanthin epoxidase gene and a novel OsTATC gene. Plant Physiol 125:1248–1257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • An P, Li X, Zheng Y, Matsuura A, Abe J, Eneji AE, Tanimoto E, Inanaga S (2014) Effects of NaCl on root growth and cell wall composition of two soybean cultivars with contrasting salt tolerance. J Agron Crop Sci 200:212–218

    Article  CAS  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Ann Rev Plant Biol 55:373–599

    Article  CAS  Google Scholar 

  • Arnon DI, McSwain BD, Tsujimoto HY, Wada K (1974) Photochemical activity and components of membrane preparation from blue-green algae. I. Coexistence of two photosystems in relation to chlorophyll a and removal of phycocyanin. Biochem Biophys Acta 357:231–245

    CAS  PubMed  Google Scholar 

  • Banno H, Chua NH (2000) Characterization of the Arabidopsis formin-like protein AFH1 and its interacting protein. Plant Cell Physiol 41:617–626

    Article  CAS  PubMed  Google Scholar 

  • Barkla B, Castellanos-Cervantes T, de Le´on JL, Matros A, Mock HP, Perez-Alfocea F, Salekdeh GH, Witzel K, Zörb C (2013) Elucidation of salt stress defense and tolerance mechanisms of crop plants using proteomics-current achievements and perspectives. Proteomics 13:1885–1900

    Article  CAS  PubMed  Google Scholar 

  • Basu B, Roychoudhury A (2014) Expression profiling of abiotic stress-inducible genes in response to multiple stresses in rice (Oryza sativa L.) varieties with contrasting level of stress tolerance. BioMed Res Int. doi:10.1155/2014/706890 (Article ID 706890)

    PubMed  PubMed Central  Google Scholar 

  • Bates L, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Burge CB, Karlin S (1998) Finding the genes in genomic DNA. Curr Op Struct Biol 8:346–354

    Article  CAS  Google Scholar 

  • Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19:371–379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doyle JJ, Doyle JL (1990) A rapid total DNA preparation procedure for fresh plant tissue. Focus 12:13–15

    Google Scholar 

  • Estrada-Melo A, Ma C, Reid MS, Jiang CZ (2015) Overexpression of an ABA biosynthesis gene using a stress-inducible promoter enhances drought resistance in petunia. Hort Res 2:15013. doi:10.1038/hortres.2015.13

    Article  Google Scholar 

  • Gomathi R, Rakkiyapan P (2011) Comparative lipid peroxidation, leaf membrane thermostability, and antioxidant system in four sugarcane genotypes differing in salt tolerance. Int J Plant Physiol Biochem 3:67–74

    CAS  Google Scholar 

  • Guerriero G, Legay S, Hausman JF (2014) Alfalfa cellulose synthase gene expression under abiotic stress: a Hitchhiker’s guide to RT-qPCR normalization. PLoS One 9(8):e103808

    Article  PubMed  PubMed Central  Google Scholar 

  • Guo A, He K, Liu D, Bai S, Gu X, Wei L, Luo J (2005) DATF: a database of Arabidopsis transcription factors. Bioinformatics 21:2568–2569

    Article  CAS  PubMed  Google Scholar 

  • Gupta B, Huang B (2014) Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int J Genom. doi:10.1155/2014/701596 (Article ID 701596)

    Google Scholar 

  • Harrington HM, Alm DM (1988) Interaction of heat and salt shock in cultured tobacco cells. Plant Physiol 88:618–625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holsters M, de Waele D, Depicker A, Messens E, van Montagu M, Schell J, Holsters M, de Waele D, Depicker A, Messens E, van Montagu M, Schell J (1978) Transfection and transformation of Agrobacterium tumefaciens. Mol Gen Genet MGG 163(2):181–187

    Article  CAS  PubMed  Google Scholar 

  • Jagadish SVK, Muthurajan R, Rang ZW, Malo R, Heuer S, Bennett J, Craufurd PQ (2011) Spikelet proteomic response to combined water deficit and heat stress in rice (Oryza sativa cv. N22). Rice 4:1–11

    Article  Google Scholar 

  • Jain M, Tyagi AK, Khurana JP (2006) Overexpression of putative topoisomerase 6 genes from rice confers stress tolerance in transgenic Arabidopsis plants. FEBS J 273:5245–5260

    Article  CAS  PubMed  Google Scholar 

  • Jefferson RA (1987) Assaying chimeric genes in plants: The GUS gene fusion system. Plant Mol Biol Rep 5:387–405

    Article  CAS  Google Scholar 

  • Jeong JS, Kim YS, Baek K, Jung H, Ha SH, Choi YD, Kim M, Reuzeau C, Kim J (2010) Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiol 153:185–197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jisha V, Dampanaboina L, Vadassery J, Mithöfer A, Kappara S, Ramanan R (2015) Overexpression of an AP2/ERF type transcription factor OsEREBP1 confers biotic and abiotic stress tolerance in rice. PLoS One 10(6):e0127831. doi:10.1371/journal.pone.0127831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kavi Kishor PB, Sreenivasulu N (2014) Is proline accumulation per se correlated with stress tolerance or is proline homoeostasis a more critical issue? Plant Cell Environ 37:300–311

    Article  CAS  PubMed  Google Scholar 

  • Kim JM, To TK, Ishida J, Matsui A, Kimura H, Seki M (2012) Transition of chromatin status during the process of recovery from drought stress in Arabidopsis thaliana. Plant Cell Physiol 53:847–856

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi Y, Yamamoto S, Minami H, Kagaya Y, Hattori T (2004) Differential activation of the rice sucrose nonfermenting1-related protein kinase2 family by hyperosmotic stress and abscisic acid. Plant Cell 16:1163–1177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63:1593–1608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krizek B (2009) AINTEGUMENTA and AINTEGUMENTA-LIKE6 act redundantly to regulate Arabidopsis floral growth and patterning. Plant Physiol 150:1916–1929

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lei Y, Song S, Fu J (2005) Possible involvement of antioxidant enzymes in the cross tolerance of the germination/growth of wheat seeds to salinity and heat stress. J Integr Plant Biol 47:1211–1219

    Article  CAS  Google Scholar 

  • Li W, Zhang C, Lu Q, Wen X, Lu C (2011) The combined effect of salt stress and heat shock on proteome profiling in Suaeda salsa. J Plant Physiol 168:1743–1752

    Article  CAS  PubMed  Google Scholar 

  • Li X, Cai J, Liu F, Dai T, Cao W, Jiang D (2014) Physiological, proteomic and transcriptional responses of wheat to combination of drought or waterlogging with late spring low temperature. Funct Plant Biol 41:690–703

    Article  CAS  Google Scholar 

  • Licausi F, Ohme-Takagi M, Perata P (2013) APETALA2/ethylene responsive factor (AP2/ERF) transcription factors: mediators of stress responses and developmental programs. New Phytol 199:639–649

    Article  CAS  PubMed  Google Scholar 

  • Lin R, Zhao W, Meng X, Wang M, Peng Y (2007) Rice gene OsNAC19 encodes a novel NAC-domain transcription factor and responds to infection by Magnaporthe grisea. Plant Sci 172:120–130

    Article  CAS  Google Scholar 

  • Ma X, Qiao Z, Chen D, Yang W, Zhou R, Zhang W, Wang M (2015) CYCLIN-DEPENDENT KINASE G2 regulates salinity stress response and salt mediated flowering in Arabidopsis thaliana. Plant Mol Biol 88:287–289

    Article  CAS  PubMed  Google Scholar 

  • Macovei A, Vaid N, Tula S, Tuteja N (2012) A new DEAD-box helicase ATP-binding protein (OsABP) from rice is responsive to abiotic stress. Plant Sign Behav 7:1138–1143

    Article  CAS  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668

    CAS  PubMed  Google Scholar 

  • Miyamoto K, Shimizu T, Mochizuki S, Nishizawa Y, Minami E, Nojiri H, Yamane H, Okada K (2013) Stress-induced expression of the transcription factor RERJ1 is tightly regulated in response to jasmonic acid accumulation in rice. Protoplasma 250:241–249

    Article  CAS  PubMed  Google Scholar 

  • Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167:645–663

    Article  CAS  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Muszynska A, Jarocka K, Kurczynska EU (2014) Plasma membrane and cell wall properties of an aspen hybrid (Populus tremula × tremuloides) parenchyma cells under the influence of salt stress. Acta Physiol Plant 36:1155–1165

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Naseri G, Sohani MM, Pourmassalehgou A, Allahi S (2012) In planta transformation of rice (Oryza sativa) using thaumatin-like protein gene for enhancing resistance to sheath blight. Afr J Biotech 11:7885–7893

    CAS  Google Scholar 

  • Negi NP, Shrivastava DC, Sharma V, Sarin NB (2015) Overexpression of CuZnSOD from Arachis hypogaea alleviates salinity and drought stress in tobacco. Plant Cell Rep 34:1109–1126

    Article  CAS  PubMed  Google Scholar 

  • Oh SJ, Kim YS, Kwon CW, Park HK, Jeong JS, Kim JK (2009) Overexpression of the transcription factor AP37 in rice improves grain yield under drought conditions. Plant Physiol 150:1368–1379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Opassiri R, Pomthong B, Akiyama T, Nakphaichit M, Onkoksoong T, Cairns MK, Cairns JRK (2007) A stress-induced rice (Oryza sativa L.) β-glucosidase represents a new subfamily of glycosyl hydrolase family 5 containing a fascin-like domain. Biochem J 408:241–249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prasch CM, Sonnewald U (2013) Simultaneous application of heat, drought, and virus to Arabidopsis plants reveals significant shifts in signaling networks. Plant Physiol 162:1849–1866

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rai M, Datta K, Parkhi V, Tan J, Oliva N, Chawla HS, Datta SK (2007) Variable T-DNA linkage configuration affects inheritance of carotenogenic transgenes and carotenoid accumulation in transgenic indica rice. Plant Cell Rep 26:1221–1231

    Article  CAS  PubMed  Google Scholar 

  • Rai M, He C, Wu R (2009) Comparative functional analysis of three abiotic stress-inducible promoters in transgenic rice. Transgenic Res 18:787–799

    Article  CAS  PubMed  Google Scholar 

  • Reddy PS, Jogeswar G, Rasineni GK, Maheswari M, Reddy AR, Varshney RK, Kavi Kishor PB (2015) Proline over-accumulation alleviates salt stress and protects photosynthetic and antioxidant enzyme activities in transgenic sorghum [Sorghum bicolor (L.) Moench]. Plant Physiol Biochem 94:104–113

    Article  PubMed  Google Scholar 

  • Rosa M, Prado C, Podazza G, Interdonato R, Gonzalez JA, Hilal M, Prado FE (2009) Soluble sugars-metabolism, sensing and abiotic stress. Plant Sign Behav 4:388–393

    Article  CAS  Google Scholar 

  • Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold inducible gene expression. Biochem Biophys Res Comm 290:998–1009

    Article  CAS  PubMed  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3:1101–1108

    Article  CAS  PubMed  Google Scholar 

  • Sewelam N, Oshima Y, Mitsuda N, Ohme-Takagi M (2014) A step towards understanding plant responses to multiple environmental stresses: a genome-wide study. Plant Cell Environ 37:2024–2035

    Article  CAS  PubMed  Google Scholar 

  • Sharoni AM, Nuruzzaman M, Satoh K, Shimizu T, Kondoh H, Sasaya T, Choi IR, Omura T, Kikuchi S (2011) Gene structures, classification and expression models of the AP2/EREBP transcription factor family in rice. Plant Cell Physiol 52:344–360

    Article  CAS  PubMed  Google Scholar 

  • Song SY, Chen Y, Chen J, Dai XY, Zhang WH (2011) Physiological mechanisms underlying OsNAC5-dependent tolerance of rice plants to abiotic stress. Planta 234:331–345

    Article  CAS  PubMed  Google Scholar 

  • Supartana P, Shimizu T, Shioiri H, Nogawa M, Nozue M, Kojima M (2005) Development of simple and efficient in planta transformation method for rice (Oryza sativa L.) using Agrobacterium tumefaciens. J Biosci Bioeng 4:391–397

    Article  Google Scholar 

  • Tao WP, Hao L, Hong Jie H, Lei W, Chun-Peng S (2011) A vacuole localized β-glucosidase contributes to drought tolerance in Arabidopsis. Chin Sci Bull 56:3538–3546

    Article  Google Scholar 

  • Todaka D, Shinozaki K, Yamaguchi-Shinozaki K (2012) Recent advances in the dissection of drought stress regulatory networks and strategies for development of drought-tolerant transgenic rice plants. Front Plant Sci 6:84. doi:10.3389/fpls.2015.00084

    Google Scholar 

  • Tuteja N, Gill SS, Tiburcio AF, Tuteja R (2012) Helicases in improving abiotic stress tolerance in crop plants. In: Tuteja N, Singh S, Tuteja R (eds) Improving crop resistance to abiotic stress, vol 1 and 2. Wiley, Hoboken. doi:10.1002/9783527632930.ch10

    Chapter  Google Scholar 

  • Wang M, Zheng Q, Shen Q, Guo S (2013) The critical role of potassium in plant stress response. Int J Mol Sci 14:7370–7390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Chai C, Valliyodan B, Maupin C, Annen B, Nguyen HT (2015) Genome-wide analysis and expression profiling of the PIN auxin transporter gene family in soybean (Glycine max). BMC Genom 16:951. doi:10.1186/s12864-015-2149-1

    Article  Google Scholar 

  • Weston DJ, Gunter LE, Rogers A, Wullschleger SD (2008) Connecting genes, coexpression modules, and molecular signatures to environmental stress phenotypes in plants. BMC Syst Biol 2:16. doi:10.1186/1752-0509-2-16

    Article  PubMed  PubMed Central  Google Scholar 

  • Xiao W, Sheen J, Jang JC (2000) The role of hexokinase in plant sugar signal transduction and growth and development. Plant Mol Biol 44:451–461

    Article  CAS  PubMed  Google Scholar 

  • Xu ZY, Lee KH, Dong T, Jeong JC, Jin JB, Kanno Y, Kim DH, Kim SY, Seo M, Bressan RA, Yun DJ, Hwang I (2012) A vacuolar β-glucosidase homolog that possesses glucose-conjugated abscisic acid hydrolyzing activity plays an important role in osmotic stress responses in Arabidopsis. Plant Cell 24:2184–2199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Y, Dong C, Li X, Du J, Qian M, Sun X, Yang Y (2016) A novel Ap2/ERF transcription factor from Stipa purpurea leads to enhanced drought tolerance in Arabidopsis thaliana. Plant Cell Rep 5:2227–2239

    Article  Google Scholar 

  • Ye N, Guohui Zhu G, Liu Y, Li Y, Zhang J (2011) ABA controls H2O2 accumulation through the induction of OsCATB in rice leaves under water stress. Plant Cell Physiol 52:689–698

    Article  CAS  PubMed  Google Scholar 

  • Yi N, Kim YS, Jeong MH, Oh SJ, Jeong JS, Park SH, Jung H, Choi Y, Kim JK (2010) Functional analysis of six drought-inducible promoters in transgenic rice plants throughout all stages of plant growth. Planta 232:743–754

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Li J, Liu A, Zou J, Zhou X, Jianhua Xiang J, Rerksiri W, Peng Y, Xiong X, Chen X (2012) Expression profile in rice panicle: insights into heat response mechanism at reproductive stage. PLoS One 7(11):e49652. doi:10.1371/journal.pone.0049652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang ZY, Li JH, Liu HH, Chong K, Xu YY (2015) Roles of ubiquitination-mediated protein degradation in plant responses to abiotic stresses. Env Exp Bot 114:92–103

    Article  CAS  Google Scholar 

  • Zhao L, Wang P, Yan S, Gao F, Li H, Hou H, Zhang Q, Tan J, Li L (2013) Promoter-associated histone acetylation is involved in the osmotic stress-induced transcriptional regulation of the maize ZmDREB2A gene. Physiol Plant 151:459–467

    Article  PubMed  Google Scholar 

  • Zhao L, Wang P, Hou H, Zhang H, Wang Y, Yan S, Huang Y, Li H, Tan J, Hu A, Gao F, Zhang Q, Li Y, Zhou H, Zhang W, Li L (2014) Transcriptional regulation of cell cycle genes in response to abiotic stresses correlates with dynamic changes in histone modifications in maize. PLoS One 9(8):e106070

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou XF, Jin YH, Yoo CY, Lin XL, Kim WY, Yun DJ, Bressan RA, Hasegawa PM, Jin JB (2013) CYCLIN H; 1 regulates drought stress responses and blue light-induced stomatal opening by inhibiting reactive oxygen species accumulation in Arabidopsis. Plant Physiol 162:1030–1041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the UGC, New Delhi (No.F.4-2/2006(BSR)/18-1(3)/2011) and CSIR, New Delhi (No.21(0934)/12/EMR-II), and we are thankful for financial assistance of the projects. MP is thankful to the UGC for providing UGC-RGNF fellowship (F. 14-2(SC)/2010(SA-III). PBK is thankful to the UGC and CSIR, New Delhi for sanctioning UGC-BSR and CSIR-Emeritus fellowships.

Author information

Authors and Affiliations

  1. Department of Genetics, Osmania University, Hyderabad, 500 007, India

    Maheshwari Parveda, D. L. Punita & P. B. Kavi Kishor

  2. Bayer BioScience Pvt. Ltd., Madhapur, Hyderabad, 500 081, India

    B. Kiran

Authors
  1. Maheshwari Parveda
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. B. Kiran
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D. L. Punita
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. P. B. Kavi Kishor
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to P. B. Kavi Kishor.

Ethics declarations

Conflict of interest

All authors have read and approved the manuscript. Authors declare no conflict of interest.

Additional information

Communicated by Nese Sreenivasulu.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 1808 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Parveda, M., Kiran, B., Punita, D.L. et al. Overexpression of SbAP37 in rice alleviates concurrent imposition of combination stresses and modulates different sets of leaf protein profiles. Plant Cell Rep 36, 773–786 (2017). https://doi.org/10.1007/s00299-017-2134-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-017-2134-z

Keywords

Search

Navigation