Abstract
Although several genes homologous to those involved in the modulation of reproductive development in the model plant Arabidopsis thaliana have been identified in the Vitis vinifera genome, the regulatory network associated with pollen development, pollen tube elongation, and fecundation in grapevine is largely unknown. In Arabidopsis, receptor kinases play essential roles in pollen tube growth and guidance, leading to proper fertilization and fruit initiation. Comparing the transcriptomic profiles of flowers and early developing berries, two grapevine genes encoding proteins with structural domains corresponding to non-RD receptor kinases were identified. The first of them, VviFTK (Vitis vinifera Flower and Tendril Kinase), is transcribed in flowers at pre-anthesis and in tendrils and shares high sequence homology with At3g03770 gene from Arabidopsis which encodes a putative phloem-specific receptor kinase of unknown function. The second gene, VviFSK (Vitis vinifera Flower and Seed Kinase), is mainly expressed in flowers at anthesis stage and in immature seeds and codes for a protein with high similarity to ScORK17, a receptor kinase involved in the ovule and seed development regulation in Solanum chacoense. VviFSK shows different expression patterns in two cultivars with opposite tendency to parthenocarpic fruit development (PFD) and its transcription is induced in response to exogenously added sucrose. In concordance with the expression mode of VviFSK, the in silico analysis of its promoter region indicates the presence of cis regulatory sequences recognized by floral homeotic transcription factors as well as elements associated with seed-specific expression and sugar induction of gene transcription. These results suggest that VviFSK protein plays a role in the seed development process in grapevine.
Similar content being viewed by others
References
Albrecht C, Russinova E, Hecht V, Baaijens E, de Vries S (2005) The Arabidopsis thaliana SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASES1 and 2 control male sporogenesis. Plant Cell 17:3337–3349
Almada R, Cabrera N, Casaretto JA, Ruiz-Lara S, González E (2009) VvCO and VvCOL1, two CONSTANS homologous genes, are regulated during flower induction and dormancy in grapevine buds. Plant Cell Rep 28:1193–1203
Alva O, Roa-Roco R, Pérez-Día R, Yáñez M, Tapia J, Moreno Y, Ruiz-Lara S, González E (2015) Pollen morphology and boron concentration in floral tissues as factors triggering natural and GA-induced parthenocarpic fruit development in grapevine. PLoS ONE 10:e0139503. https://doi.org/10.1371/journal.pone.0139503
Aziz A (2003) Spermidine and related-metabolic inhibitors modulate sugar and amino acid levels in Vitis vinifera L.: possible relationships with initial fruitlet abscission. J Exp Bot 54:355–363
Becraft P (2002) Receptor kinase signaling in plant development. Annu Rev Cell Dev Biol 18:163–192. https://doi.org/10.1146/annurev.cellbio.18.012502.083431
Bendtsen J, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340:783–795
Blom N, Gammeltoft S, Brunak S (1999) Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J Mol Biol 294:1351–13623
Boss P, Thomas M (2000) Tendrils, inflorescences and fruitfulness: a molecular perspective. Aust J Grape Wine Res 6:168–174
Calonje M, Cubas P, Martínez-Zapater JM, Carmona MJ (2004) Floral meristem identity genes are expressed during tendril development in grapevine. Plant Physiol 135:1491–1501
Canales C, Bhatt AM, Scott R, Dickinson H (2002) EXS, a putative LRR receptor kinase, regulates male germline cell number and tapetal identity and promotes seed development in Arabidopsis. Curr Biol 12:1718–1727
Carmona MJ, Chaïb J, Martínez-Zapater JM, Thomas MR (2008) A molecular genetic perspective of reproductive development in grapevine. J Exp Bot 59:2579–2596
Castells E, Casacuberta JM (2007) Signalling through kinase-defective domains: the prevalence of atypical receptor-like kinases in plants. J Exp Bot 58:3503–3511
Colcombert J, Boisson-Dernier A, Ros-Palau R, Vera C, Schroeder J (2005) Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASES1 and 2 are essential for tapetum development and microspore maturation. Plant Cell 17:3350–3361
Colin L, Cholet C, Geny L (2002) Relationships between endogenous polyamines, cellular structure and arrested growth of grape berries. Aust J Grape Wine Res 8:101–108
Coombe B (1995) Growth stages of the grapevine: adoption of a system for identifying grapevine growth stages. Aust J Grape Wine Res 1:104–110
Dardick C, Ronald P (2006) Plant and animal pathogen recognition receptors signal through non-RD kinases. PLoS Pathog 2:e2
Dardick C, Schwessinger B, Ronald P (2012) Non-arginine-aspartate (non-RD) kinases are associated with innate immune receptors that recognize conserved microbial signatures. Curr Opin Plant Biol 15:358–366
DeYoung BJ, Bickle KL, Schrage KJ, Muskett P, Patel K, Clark S (2006) The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis. Plant J 45:1–16
Díaz-Riquelme J, Martínez-Zapater JM, Carmona MJ (2014) Transcriptional analysis of tendril and inflorescence development in grapevine (Vitis vinifera L.). PLoS ONE 9:e92339
Dresselhaus T, Franklin-Tong N (2013) Male-female crosstalk during pollen germination, tube growth and guidance, and double fertilization. Mol Plant 6:1018–1036. https://doi.org/10.1093/mp/sst061
Escobar-Restrepo JM, Huck N, Kessler S, Gagliardini V, Gheyselinck J, Yang WC, Grossniklaus U (2007) The FERONIA receptor-like kinase mediates male-female interactions during pollen tube reception. Science 317:656–660. https://doi.org/10.1126/science.1143562
Fernández J, Talle B, Wilson Z (2015) Anther and pollen development: a conserved developmental pathway. J Integr Plant Biol 57:876–891
Franklin-Tong N (2010) Plant fertilization: bursting pollen tubes! Curr Biol 20:R681-683. https://doi.org/10.1016/j.cub.2010.06.038
Gärtel W (1993) Grapes. In: Bennett WF (ed) Nutrient deficiencies and toxicities in crop plants. APS Press, St. Paul, pp 177–183
Gasteiger E, Gattiker A, Hoogland C, Ivanyi I, Appel RD, Bairoch A (2003) ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res 31:3784–3788
Germain H, Houde J, Gray-Mitsumune M, Sawasaki T, Endo Y, Rivoal J, Matton DP (2007) Characterization of ScORK28, a transmembrane functional protein receptor kinase predominantly expressed in ovaries from the wild potato species Solanum chacoense. FEBS Lett 581:5137–5142
Germain H, Gray-Mitsumune M, Lafleur E, Matton DP (2008) ScORK17, a transmembrane receptor-like kinase predominantly expressed in ovules is involved in seed development. Planta 228:851–862
Gish LA, Clark SE (2011) The RLK/Pelle family of kinases. Plant J 66:117–127
Gong J, Wei T, Zhang N, Jamitzky F, Heckl WM, Rössle SC, Stark RW (2010) TollML: a database of toll-like receptor structural motifs. J Mol Model 16:1283–1289
Hanks SK, Hunter T (1995) Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J 9:576–596
Hanks SK, Quinn AM, Hunter T (1988) The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241:42–52
Hecht V, Vielle-Calzada J-P, Hartog MV, Schmidt ED, Boutilier K, Grossniklaus U, de Vries SC (2001) The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE 1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture. Plant Physiol 127:803–816
Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27:297–300
Hord C, Chen C, Deyoung B, Clark S, Ma H (2006) The BAM1/BAM2 receptor like-kinases are important regulators of Arabidopsis early anther development. Plant Cell 18:1667–1680
Horton P, Park K-J, Obayashi T, Fujita N, Harada H, Adams-Collier C, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:W585–W587
Hunter S et al (2009) InterPro: the integrative protein signature database. Nucleic Acids Res 37:D211–D215
Ito T, Wellmer F, Yu H, Das P, Ito N, Alves-Ferreira M, Riechmann J, Meyerowitz E (2004) The homeotic protein AGAMOUS controls microsporogenesis by regulation of SPOROCYTELESS. Nature 430:356–360
Jung CJ, Hur YY, Yu H-J, Noh J-H, Park K-S, Lee HJ (2014) Gibberellin application at pre-bloom in grapevines down-regulates the expressions of VvIAA9 and VvARF7, negative regulators of fruit set initiation, during parthenocarpic fruit development. PLoS ONE 9:e95634
Käll L, Krogh A, Sonnhammer EL (2004) A combined transmembrane topology and signal peptide prediction method. J Mol Biol 338:1027–1036
Kanaoka M, Higashiyama T (2015) Peptide signaling in pollen tube guidance. Curr Opin Plant Biol 28:127–136
Keller M (2005) Deficit irrigation and vine mineral nutrition. Am J Enol Vitic 56:267–283
Keller M (2010) Managing grapevines to optimise fruit development in a challenging environment: a climate change primer for viticulturists. Aust J Grape Wine Res 16:56–69
Kessler SA, Shimosato-Asano H, Keinath NF, Wuest SE, Ingram G, Panstruga R, Grossniklaus U (2010) Conserved molecular components for pollen tube reception and fungal invasion. Science 330:968–971
Krogh A, Larsson B, Von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580
Kühn N, Arce-Johnson P (2012) Pollination: A key event controlling the expression of genes related to phytohormone biosynthesis during grapevine berry formation. Plant Signal Behav 7:7–11
Li J (2011) Direct involvement of leucine-rich repeats in assembling ligand-triggered receptor-coreceptor complexes. Proc Natl Acad Sci USA 108:8073–8074. https://doi.org/10.1073/pnas.1104057108
Li L, Sheen J (2016) Dynamic and diverse sugar signaling. Curr Opin Plant Biol 33:116–125
Li H, Yang W (2016) RLKs orchestrate the signaling in plant male-female interaction. Sci China Life Sci 59:867–877
Li C, Wu H, Cheung A (2016) FERONIA and her pals: functions and mechanisms. Plant Physiol 171:2379–2392
Li Z, Zhang C, Guo Y, Niu W, Wang Y, Xu Y (2017) Evolution and expression analysis reveal the potential role of the HD-Zip gene family in regulation of embryo abortion in grapes (Vitisvinifera L.). BMC Genom 18:744
Miyazaki S, Murata T, Sakurai-Ozato N, Kubo M, Demura T, Fukuda H, Hasebe M (2009) ANXUR1 and 2, sister genes to FERONIA/SIRENE, are male factors for coordinated fertilization. Curr Biol 19:1327–1331. https://doi.org/10.1016/j.cub.2009.06.064
Mullins MG, Bouquet A, Williams LE (1992) Biology of the grapevine. Cambridge University Press, Cambridge, pp 107–110
Muschietti J, Wengier D (2018) How many receptor-like kinases are required to operate a pollen tube. Curr Opin Plant Biol 41:73–82
Nodine MD, Bryan AC, Racolta A, Jerosky KV, Tax FE (2011) A few standing for many: embryo receptor-like kinases. Trends Plant Sci 16:211–217. https://doi.org/10.1016/j.tplants.2011.01.005
Obenauer JC, Cantley LC, Yaffe MB (2003) Scansite 2.0: proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res 31:3635–3641
Peña-Cortés H et al (2005) Chilean effort for improving fruit quality in grapevine: a genomic approach to understanding seed formation, fruit ripening and pathogen response. Acta Hort 689:505
Reid KE, Olsson N, Schlosser J, Peng F, Lund ST (2006) An optimized grapevine RNA isolation procedure and statistical determination of reference genes for real-time RT-PCR during berry development. BMC Plant Biol 6:1
Ruiz-Medrano R, Xoconostle-Cazares B, Ham BK, Li G, Lucas WJ (2011) Vascular expression in Arabidopsis is predicted by the frequency of CT/GA-rich repeats in gene promoters. Plant J 67:130–144. https://doi.org/10.1111/j.1365-313X.2011.04581.x
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Sandelin A, Wasserman WW, Lenhard B (2004) ConSite: web-based prediction of regulatory elements using cross-species comparison. Nucleic Acids Res 32:W249–W252
Schultz J, Milpetz F, Bork P, Ponting CP (1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci 95:5857–5864
Shatkay H, Höglund A, Brady S, Blum T, Dönnes P, Kohlbacher O (2007) SherLoc: high-accuracy prediction of protein subcellular localization by integrating text and protein sequence data. Bioinformatics 23:1410–1417
Shiu S-H, Karlowski WM, Pan R, Tzeng Y-H, Mayer KF, Li W-H (2004) Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16:1220–1234
Takeuchi H, Higashiyama T (2016) Tip-localized receptors control pollen tube growth and LURE sensing in Arabidopsis. Nature 531:245–248
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
Team RC (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, p 2013
Thompson J, Gibson T, Plewniak F, Jeanmougin F, Higgins D (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Tucker SC, Hoefert L (1968) Ontogeny of the tendril in Vitis vinifera. Am J Bot 55:1110–1119
Vasconcelos M, Greven M, Winefield C, Trought M, Raw V (2009) The flowering process of Vitisvinifera: a review. Am J Enol Vitic 60:411–434
Wang T, Liang L, Xue Y, Jia P, Chen W, Zhang M, Wang Y, Li H, Yang W (2016) A receptor heteromer mediates the male perception of female attractants in plants. Nature 531:241–244
Weaver R, McCune S, Hale C (1962) Effect of plant regulators on set and berry development in certain seedless varieties of Vitisvinifera L. Vitis 3:84–96
Wigge P, Kim M, Jaeger K, Busch W, Schmid M, Lohmann J, Weigel D (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309:1056–1059
Wijeratne A, Zhang W, Sun Y, Liu W, Albert R, Zheng Z, Oppenheimer D, Zhao D, Ma H (2007) Differential gene expression in Arabidopsis wild-type and mutant anthers: insights into anther cell differentiation and regulatory networks. Plant J 52:14–29
Wilson Z, Zhang D (2009) From Arabidopsis to rice: pathways in pollen development. J Exp Botany 60:1479–1492
Yan W, Chen D, Kaufmann K (2016) Molecular mechanisms of floral organ specification by MADS domain proteins. Curr Opin Plant Biol 29:154–162. https://doi.org/10.1016/j.pbi.2015.12.004
Yu C, Chen Y, Lu C, Hwang J (2006) Prediction of protein subcellular localization. Proteins Struct Funct Bioinform 64:643–651
Zhang N, Wen J, Zimmer EA (2015) Expression patterns of AP1, FUL, FT and LEAFY orthologs in Vitaceae support the homology of tendrils and inflorescences throughout the grape family. J Syst Evol 53:469–476. https://doi.org/10.1111/jse.12138
Acknowledgements
This work was supported by Fondo Nacional de Desarrollo Científico y Tecnológico (FONDECYT) Grant 1161237. S. González was supported by Comisión Nacional de Investigación Científica y Tecnológica (CONICYT) doctoral fellowship.
Author information
Authors and Affiliations
Contributions
All the authors contributed to the design and implementation of the research, the analysis of the results, and the writing of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Additional information
Handling Editor: Rhonda Peavy.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
344_2021_10346_MOESM4_ESM.docx
Supplementary figure 1 Nucleotide sequence of the EST VVCCGS2117F10.b identified in a cDNA library obtained from small berries of grapevine with homology to At3g03770 from A. thaliana. Supplementary file4 (DOCX 13 KB)
Rights and permissions
About this article
Cite this article
González, S.A., Pérez-Díaz, R., González-Villanueva, E. et al. VviFSK and VviFTK, Two Novel Genes Encoding Putative Non-RD Receptor Kinases Associated with Reproductive Development in Grapevine. J Plant Growth Regul 41, 875–888 (2022). https://doi.org/10.1007/s00344-021-10346-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-021-10346-x