Skip to main content
SpringerLink
Log in

Genome-wide analyses of banana fasciclin-like AGP genes and their differential expression under low-temperature stress in chilling sensitive and tolerant cultivars

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

Abstract

Key messages

Thirty MaFLAs vary in their molecular features. MaFLA14/18/27/29 are likely to be involved in banana chilling tolerance by facilitating the cold signaling pathway and enhancing the cell wall biosynthesis.

Abstract

Although several studies have identified the molecular functions of individual fasciclin-like arabinogalactan protein (FLA) genes in plant growth and development, little information is available on their involvement in plant tolerance to low-temperature (LT) stress, and the related underlying mechanism is far from clear. In this study, the different expression of FLAs of banana (Musa acuminata) (MaFLAs) in the chilling-sensitive (CS) and chilling-tolerant (CT) banana cultivars under natural LT was investigated. Based on the latest banana genome database, a genome-wide identification of this gene family was done and the molecular features were analyzed. Thirty MaFLAs were distributed in 10 out of 11 chromosomes and these clustered into four major phylogenetic groups based on shared gene structure. Twenty-four MaFLAs contained N-terminal signal, 19 possessed predicted glycosylphosphatidylinositol (GPI), while 16 had both. Most MaFLAs were downregulated by LT stress. However, MaFLA14/18/29 were upregulated by LT in both cultivars with higher expression level recorded in the CT cultivar. Interestingly, MaFLA27 was significantly upregulated in the CT cultivar, but the opposite occurred for the CS cultivar. MaFLA27 possessed only N-terminal signal, MaFLA18 contained only GPI anchor, MaFLA29 possessed both, while MaFLA14 had neither. Thus, it was suggested that the accumulation of these FLAs in banana under LT could improve banana chilling tolerance through facilitating cold signal pathway and thereafter enhancing biosynthesis of plant cell wall components. The results provide background information of MaFLAs, suggest their involvement in plant chilling tolerance and their potential as candidate genes to be targeted when breeding CT banana.

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

Similar content being viewed by others

Abbreviations

AG:

Arabinogalactan

AGPs:

Arabinogalactan proteins

CS:

Chilling-sensitive

CT:

Chilling-tolerant

ECM:

Extracellular matrix

FLAs:

Fasciclin-like AGPs

GPI:

Glycosylphosphatidylinositol

HRGPs:

Hydroxyproline-rich glycoproteins

IF:

Immunofluorescence

GPI-APs:

GPI-anchored proteins

Ka:

Nonsynonymous substitution rate

Ks:

Synonymous substitution rate

LT:

Low temperature

MEME:

Multiple Em for Motif Elucidation

NJ:

Neighbor-joining

pI:

Isoelectric point

PVDF:

Polyvinylidene difluoride

qPCR:

Quantitative real-time PCR

REC:

Relative electrical conductivity

RLKs:

Receptor-like kinases

TBST:

Tris-buffered saline Tween-20

References

  • Bailey TL, Elkan C (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Int Conf Intell Syst Mol Biol 2:28–36

    CAS  Google Scholar 

  • Basu D, Tian L, Debrosse T, Poirier E, Emch K, Herock H, Travers A, Showalter AM (2016) Glycosylation of a fasciclin-like arabinogalactan-protein (SOS5) mediates root growth and seed mucilage adherence via a cell wall receptor-like kinase (FEI1/FEI2) pathway in Arabidopsis. PLoS ONE 11:e0145092

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cagnola JI, de Chassart GJD, Ibarra SE, Chimenti C, Ricardi MM, Delzer B, Ghiglione H, Zhu T, Otegui ME, Estevez JM, Casal JJ (2018) Reduced expression of selected FASCICLIN-LIKE ARABINOGALACTAN PROTEIN genes associates with the abortion of kernels in field crops of Zea mays (maize) and of Arabidopsis seeds. Plant Cell Environ 41:661–674

    Article  PubMed  CAS  Google Scholar 

  • Cao S, Bian K, Shi L, Chung HH, Chen W, Yang Z (2018) Role of melatonin in cell-wall disassembly and chilling tolerance in cold-stored peach fruit. J Agric Food Chem 66:5663–5670

    Article  PubMed  CAS  Google Scholar 

  • Chen L, Zhong H, Kuang J, Lu W, Chen J (2011) Validation of reference genes for RT-qPCR studies of gene expression in banana fruit under different experimental conditions. Planta 234:377–390

    Article  PubMed  CAS  Google Scholar 

  • Chinnusamy V, Zhu J, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12:444–451

    Article  PubMed  CAS  Google Scholar 

  • D’Hont A, Denoeud F, Aury JM et al (2012) The banana (Musa acuminata) genome and the evolution of monocotyledonous plants. Nature 488:213–217

    Article  PubMed  CAS  Google Scholar 

  • Eddy SR (1998) Profile hidden Markov models. Bioinformatics 14:755–763

    Article  PubMed  CAS  Google Scholar 

  • Eisenhaber B, Wildpaner M, Schultz CJ, Borner GH, Dupree P, Eisenhaber F (2003) Glycosylphosphatidylinositol lipid anchoring of plant proteins. Sensitive prediction from sequence-and genome-wide studies for Arabidopsis and rice. Plant Physiol 133:1691–1701

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ellis C, Karafyllidis I, Wasternack C, Turner JG (2002) The Arabidopsis mutant cev1 links cell wall signaling to jasmonate and ethylene responses. Plant Cell 14:1557–1566

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ellis M, Egelund J, Schultz CJ, Bacic A (2010) Arabinogalactan-proteins: key regulators at the cell surface? Plant Physiol 153:403–419

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Faik A, Abouzouhair J, Sarhan F (2006) Putative fasciclin-like arabinogalactan-proteins (FLA) in wheat (Triticum aestivum) and rice (Oryza sativa): identification and bioinformatic analyses. Mol Genet Genom 276:478–494

    Article  CAS  Google Scholar 

  • FAOSTAT (2019). https://www.fao.org/faostat/en/#data/QC/visualize

  • Feng R, Zhang L, Wang J, Luo J, Peng M, Qi J, Zhang Y, Lu L (2015) Proteomic analysis of cold stress responses in banana leaves. J Am Soc Hortic Sci 140:214–222

    Article  CAS  Google Scholar 

  • Gaspar Y, Johnson KL, McKenna JA, Bacic A, Schultz CJ (2001) The complex structures of arabinogalactan-proteins and the journey towards understanding function. Plant Mol Biol 47:161–176

    Article  PubMed  CAS  Google Scholar 

  • Guerriero G, Mangeot-Peter L, Legay S, Behr M, Lutts S, Siddiqui K, Hausman J (2017) Identification of fasciclin-like arabinogalactan proteins in textile hemp (Cannabis sativa L.): in silico analyses and gene expression patterns in different tissues. BMC Genom 18:741

    Article  CAS  Google Scholar 

  • Harris TJC, Siu CH (2002) Reciprocal raft-receptor interactions and the assembly of adhesion complexes. BioEssays 24:996–1003

    Article  PubMed  CAS  Google Scholar 

  • He J, Zhao H, Cheng Z, Ke Y, Liu J, Ma H (2019) Evolution analysis of the fasciclin-like arabinogalactan proteins in plants shows variable fasciclin-AGP domain constitutions. Int J Mol Sci 20:1945

    Article  PubMed Central  CAS  Google Scholar 

  • Hu B, Jin J, Guo A, Zhang H, Luo J, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297

    Article  PubMed  Google Scholar 

  • Huang G, Xu W, Gong S, Li B, Wang X, Xu D, Li X (2008) Characterization of 19 novel cotton FLA genes and their expression profiling in fiber development and in response to phytohormones and salt stress. Physiol Plant 134:348–359

    Article  PubMed  CAS  Google Scholar 

  • Huang G, Gong S, Xu W, Li W, Li P, Zhang C, Li D, Zheng Y, Li F, Li X (2013) A fasciclin-like arabinogalactan protein, GhFLA1, is involved in fiber initiation and elongation of cotton. Plant Physiol 161:1278–1290

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Huang X, Ji Z, Li P (1982) A study on the injury symptoms and physiological quota of banana and an effective measure for cold injury protection. J South China Agric Univ 3:1–12 (in Chinese with an English abstract)

    Google Scholar 

  • Hurst LD (2002) The Ka/Ks ratio: diagnosing the form of sequence evolution. Trends Genet 18:486–487

    Article  PubMed  Google Scholar 

  • Ji H, Wang Y, Cloix C, Li K, Jenkins GI, Wang S, Shang Z, Shi Y, Yang S, Li X (2015) The Arabidopsis RCC1 family protein TCF1 regulates freezing tolerance and cold acclimation through modulating lignin biosynthesis. PLoS Genet 11:e1005471

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Johnson KL, Jones BJ, Bacic A, Schultz CJ (2003) The fasciclin-like arabinogalactan proteins of Arabidopsis. A multigene family of putative cell adhesion molecules. Plant Physiol 133:1911–1925

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Johnson KL, Kibble NA, Bacic A, Schultz CJ (2011) A fasciclin-like arabinogalactan-protein (FLA) mutant of Arabidopsis thaliana, fla1, shows defects in shoot regeneration. PLoS ONE 6:e25154

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lafarguette F, Pilate G (2004) Poplar genes encoding fasciclin-like arabinogalactan proteins are highly expressed in tension wood. New Phytol 164:107–121

    Article  CAS  PubMed  Google Scholar 

  • Letunic I, Doerks T, Bork P (2012) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res 40:302–305

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Li J, Wu XM (2012) Genome-wide identification, classification and expression analysis of genes encoding putative fasciclin-like arabinogalactan proteins in Chinese cabbage (Brassica rapa L.). Mol Biol Rep 39:10541–10555

    Article  CAS  Google Scholar 

  • Li S, Yang Y, Zhang Q, Liu N, Xu Q, Hu L (2018) Differential physiological and metabolic response to low temperature in two zoysiagrass genotypes native to high and low latitude. PLoS ONE 13:e0198885

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu W, Cheng C, Lin Y, XuHan X, Lai Z (2018) Genome-wide identification and characterization of mRNAs and lncRNAs involved in cold stress in the wild banana (Musa itinerans). PLoS ONE 13:e200002

    Google Scholar 

  • Ma H, Zhao J (2010) Genome-wide identification, classification, and expression analysis of the arabinogalactan protein gene family in rice (Oryza sativa L.). J Exp Bot 61:2647–2668

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ma Y, Yan C, Li H, Wu W, Liu Y, Wang Y, Chen Q, Ma H (2017) Bioinformatics prediction and evolution analysis of arabinogalactan proteins in the plant kingdom. Front Plant Sci 8:66

    PubMed  PubMed Central  Google Scholar 

  • MacMillan CP, Mansfield SD, Stachurski ZH, Evans R, Southerton SG (2010) Fasciclin-like arabinogalactan proteins: specialization for stem biomechanics and cell wall architecture in Arabidopsis and Eucalyptus. Plant J 62:689–703

    Article  PubMed  CAS  Google Scholar 

  • MacMillan CP, Taylor L, Bi Y, Southerton SG, Evans R, Spokevicius A (2015) The fasciclin-like arabinogalactan protein family of Eucalyptus grandis contains members that impact wood biology and biomechanics. New Phytol 206:1314–1327

    Article  PubMed  CAS  Google Scholar 

  • Majewska-Sawka A, Nothnagel EA (2000) The multiple roles of arabinogalactan proteins in plant development. Plant Physiol 122:3–9

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mareri L, Romi M, Cai G (2019) Arabinogalactan proteins: actors or spectators during abiotic and biotic stress in plants? Plant Biosyst 153:173–185

    Article  Google Scholar 

  • Mashiguchi K, Urakami E, Hasegawa M, Sanmiya K, Matsumoto I, Yamaguchi I, Asami T, Suzuki Y (2008) Defense-related signaling by interaction of arabinogalactan proteins and beta-glucosyl Yariv reagent inhibits gibberellin signaling in barley aleurone cells. Plant Cell Physiol 49:178–190

    Article  PubMed  CAS  Google Scholar 

  • Niu Y, Hu B, Li X, Chen H, Takáč T, Šamaj J, Xu C (2018) Comparative digital gene expression analysis of tissue-cultured plantlets of highly resistant and susceptible banana cultivars in response to Fusarium oxysporum. Int J Mol Sci 19:350

    Article  PubMed Central  CAS  Google Scholar 

  • No EG, Loopstra CA (2000) Hormonal and developmental regulation of two arabinogalactan-proteins in xylem of loblolly pine (Pinus taeda). Physiol Plant 110:524–529

    Article  CAS  Google Scholar 

  • Perrier X, De Langhe E, Donohue M, Lentfer C, Vrydaghs L, Bakry F, Carreel F, Hippolyte I, Horry JP, Jenny C, Lebot V, Risterucci AM, Tomekpe K, Doutrelepont H, Ball T, Manwaring J, de Maret P, Denham T (2011) Multidisciplinary perspectives on banana (Musa spp.) domestication. Proc Natl Acad Sci 108:11311–11318

    Article  PubMed  PubMed Central  Google Scholar 

  • Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785–786

    Article  PubMed  CAS  Google Scholar 

  • Schultz CJ, Rumsewicz MP, Johnson KL, Jones BJ, Gaspar YM, Bacic A (2002) Using genomic resources to guide research directions. The arabinogalactan protein gene family as a test case. Plant Physiol 129:1448–1463

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Seifert GJ, Roberts K (2007) The biology of arabinogalactan proteins. Annu Rev Plant Biol 58:137–161

    Article  PubMed  CAS  Google Scholar 

  • Seifert GJ, Xue H, Acet T (2014) The Arabidopsis thaliana FASCICLIN LIKE ARABINOGALACTAN PROTEIN 4 gene acts synergistically with abscisic acid signaling to control root growth. Ann Bot 114:1125–1133

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shi H, Kim Y, Guo Y, Stevenson B, Zhu JK (2003) The Arabidopsis SOS5 locus encodes a putative cell surface adhesion protein and is required for normal cell expansion. Plant Cell 15:19–32

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Showalter AM (2001) Arabinogalactan-proteins: structure, expression and function. Cell Mol Life Sci 58:1399–1417

    Article  PubMed  CAS  Google Scholar 

  • Showalter AM, Keppler B, Lichtenberg J, Gu D, Welch LR (2010) A bioinformatics approach to the identification, classification, and analysis of hydroxyproline-rich glycoproteins. Plant Physiol 153:485–513

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Showalter AM, Keppler BD, Liu X, Lichtenberg J, Welch LR (2016) Bioinformatic identification and analysis of hydroxyproline-rich glycoproteins in Populus trichocarpa. BMC Plant Biol 16:229

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sukumaran NP, Weiser CJ (1972) An excised leaflet test for evaluating potato frost tolerance. HortScience 7:467–468

    Google Scholar 

  • Takahashi D, Kawamura Y, Uemura M (2013) Changes of detergent-resistant plasma membrane proteins in oat and rye during cold acclimation: association with differential freezing tolerance. J Proteome Res 12:4998–5011

    Article  PubMed  CAS  Google Scholar 

  • Takahashi D, Kawamura Y, Uemura M (2016) Cold acclimation is accompanied by complex responses of glycosylphosphatidylinositol (GPI)-anchored proteins in Arabidopsis. J Exp Bot 67:5203–5215

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Turner DW, Lahav E (1983) The growth of banana plants in relation to temperature. Funct Plant Biol 10:43–53

    Article  Google Scholar 

  • Turupcu A, Almohamed W, Oostenbrink C, Seifert GJ (2018) A speculation on the tandem fasciclin 1 repeat of FLA4 proteins in angiosperms. Plant Signal Behav 13:e1507403

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Van Holle S, Van Damme EJM (2018) Signaling through plant lectins: modulation of plant immunity and beyond. Biochem Soc Trans 46:217–233

    Article  PubMed  CAS  Google Scholar 

  • Wang H, Jiang C, Wang C, Yang Y, Yang L, Gao X, Zhang H (2015) Antisense expression of the fasciclin-like arabinogalactan protein FLA6 gene in Populus inhibits expression of its homologous genes and alters stem biomechanics and cell wall composition in transgenic trees. J Exp Bot 66:1291–1302

    Article  PubMed  CAS  Google Scholar 

  • Xie D, Ma L, Šamaj J, Xu C (2011) Immunohistochemical analysis of cell wall hydroxyproline-rich glycoproteins in the roots of resistant and susceptible wax gourd cultivars in response to Fusarium oxysporum f. sp. Benincasae infection and fusaric acid treatment. Plant Cell Rep 30:1555–1569

    Article  PubMed  CAS  Google Scholar 

  • Xu C, Takáč T, Burbach C, Menzel D, Šamaj J (2011) Developmental localization and the role of hydroxyproline rich glycoproteins during somatic embryogenesis of banana (Musa spp. AAA). BMC Plant Biol 11:38

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xue H, Seifert GJ (2015) FASCICLIN LIKE ARABINOGALACTAN PROTEIN 4 and RESPI RATORY BURST OXIDASE HOMOLOG D and F independently modulate abscisic acid signaling. Plant Signal Behav 10:e989064

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xue H, Veit C, Abas L, Tryfona T, Maresch D, Ricardi MM, Estevez JM, Strasser R, Seifert GJ (2017) Arabidopsis thaliana FLA4 functions as a glycan-stabilized soluble factor via its carboxy-proximal fasciclin 1 domain. Plant J 91:613–630

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yan Y, Takáč T, Li X, Chen H, Wang Y, Xu E, Xie L, Su Z, Šamaj J, Xu C (2015) Variable content and distribution of arabinogalactan proteins in banana (Musa spp.) under low temperature stress. Front Plant Sci 6:353

    PubMed  PubMed Central  Google Scholar 

  • Yang Q, Gao J, He W, Dou T, Ding L, Wu J, Li C, Peng X, Zhang S, Yi G (2015) Comparative transcriptomics analysis reveals difference of key gene expression between banana and plantain in response to cold stress. BMC Genom 16:446

    Article  CAS  Google Scholar 

  • Yang Q, Wu J, Li C, Wei Y, Sheng O, Hu C, Kuang R, Huang Y, Peng X, McCardle JA, Chen W, Yang Y, Rose JKC, Zhang S, Yi G (2012) Quantitative proteomic analysis reveals that antioxidation mechanisms contribute to cold tolerance in plantain (Musa paradisiaca L.; ABB Group) seedlings. Mol Cell Proteom 11:1853–1869

    Article  CAS  Google Scholar 

  • Zang L, Zheng T, Chu Y, Ding C, Zhang W, Huang Q, Su X (2015) Genome-wide analysis of the fasciclin-like arabinogalactan protein gene family reveals differential expression patterns, localization, and salt stress response in Populus. Front Plant Sci 6:1140

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou K (2019) Glycosylphosphatidylinositol-anchored proteins in Arabidopsis and one of their common roles in signaling transduction. Front Plant Sci 10:1022

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Key Research and Development Program of China (2018YFD1000300), the Key Research and Development Program of Guangdong Province for Modern Plant Breeding (2018B020202005), the Guangdong Province Special Fund for Modern Agriculture Industry Technology Innovation Teams, the Earmarked Fund for Modern Agro-industry Technology Research System (CARS-31-04).

Author information

Authors and Affiliations

  1. College of Horticulture, South China Agricultural University, Guangzhou, 510642, China

    Jian Meng, Bei Hu, Houbin Chen, Yingying Wang, Weina Yuan, Yanqing Xing, Qiming Sheng & Chunxiang Xu

  2. Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, China

    Ganjun Yi

  3. Institute of Biotechnology, Guangxi Academy of Agricultural Sciences, Nanning, 530007, China

    Xiaoquan Li & Zuxiang Su

Authors
  1. Jian Meng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bei Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ganjun Yi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiaoquan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Houbin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yingying Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Weina Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yanqing Xing
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Qiming Sheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Zuxiang Su
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Chunxiang Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chunxiang Xu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Kinya Toriyama.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOC 2396 kb)

Supplementary file2 (DOCX 362 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Meng, J., Hu, B., Yi, G. et al. Genome-wide analyses of banana fasciclin-like AGP genes and their differential expression under low-temperature stress in chilling sensitive and tolerant cultivars. Plant Cell Rep 39, 693–708 (2020). https://doi.org/10.1007/s00299-020-02524-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-020-02524-0

Keywords

Search

Navigation