Plant Protect. Sci., 2022, 58(2):125-138 | DOI: 10.17221/131/2021-PPS

Genome-wide characterisation, evolution and expression analysis of the leucine-rich repeat receptor-like kinase (LRR-RLK) gene family in cucumbersOriginal Paper

Jia Yu, Bo Zhang, Sisi Liu, Wei Guo, Yifan Gao, Hongyan Sun ORCID...*
College of Chemical and Biological Engineering, Taiyuan University of Science and Technology, Taiyuan, P.R. China

The leucine-rich repeat receptor-like kinases (LRR-RLKs) compose a large gene family in plant genomes and implement essential functions in diverse plant physiology progress, including defence against pathogens. However, a systematic analysis of LRR-RLKs has not been accomplished in the economically important cucumber. 189 LRR-RLK genes were identified in the cucumber genome and further divided into 22 subgroups based on the sequence similarities in this study. A total of 31 segmental duplication events and 15 tandem duplication events were present in the genome, indicating that the two duplications were the main driving forces for the expansion of the LRR-RLK family in the cucumber. The expression profile analysis revealed that most of the CsLRR-RLKs were upregulated during a downy mildew infection, and resistant cucumbers comprised more upregulated CsLRR-RLKs than the sensitive lines. Taken together, our results provided information on the LRR-RLK gene family in the cucumber and contributed valuable information for the further research of CsLRR-RLKs.

Keywords: Cucumis sativus; evolutionary analysis; gene expression; genome sequence; Pseudoperonospora cubensis

Published: March 28, 2022  Show citation

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Yu J, Zhang B, Liu S, Guo W, Gao Y, Sun H. Genome-wide characterisation, evolution and expression analysis of the leucine-rich repeat receptor-like kinase (LRR-RLK) gene family in cucumbers. Plant Protect. Sci. 2022;58(2):125-138. doi: 10.17221/131/2021-PPS.
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    References

    1. Alcázar R., García A.V., Kronholm I., de Meaux J., Koornneef M., Parker J.E., Reymond M. (2010): Natural variation at Strubbelig Receptor Kinase3 drives immune-triggered incompatibilities between Arabidopsis thaliana accessions. Nature Genetics, 42: 1135-1139. Go to original source... Go to PubMed...
    2. Asai T., Tena G., Plotnikova J., Willmann M.R., Chiu W.L., Gomez-Gomez L., Boller T., Ausubel F.M., Sheen J. (2002): MAP kinase signalling cascade in Arabidopsis innate immunity. Nature, 415: 977-983. Go to original source... Go to PubMed...
    3. Bailey T.L., Williams N., Misleh C., Li W.W. (2006): MEME: Discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Research, 34: W369-W373. Go to original source... Go to PubMed...
    4. Burkhardt A., Day B. (2016): Transcriptome and small rnaome dynamics during a resistant and susceptible interaction between cucumber and downy mildew. Plant Genome, 9. doi: 10.3835/plantgenome2015.08.0069 Go to original source... Go to PubMed...
    5. Camacho C., Coulouris G., Avagyan V., Ma N., Papadopoulos J., Bealer K., Madden T.L. (2009): BLAST+: Architecture and applications. BMC Bioinformatics, 10. doi: 10.1186/1471-2105-10-421 Go to original source... Go to PubMed...
    6. Cao Y., Mo W., Li Y., Li W., Dong X., Liu M., Jiang L., Zhang L. (2021): Deciphering the roles of leucine-rich repeat receptor-like protein kinases (LRR-RLKs) in response to Fusarium wilt in the Vernicia fordii (Tung tree). Phytochemistry, 185. doi: 10.1016/j.phytochem.2021.112686 Go to original source... Go to PubMed...
    7. Chinchilla D., Bauer Z., Regenass M., Boller T., Felix G. (2006): The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell, 18: 465-476. Go to original source... Go to PubMed...
    8. Expósito R.R., González-Domínguez J., Touriño J. (2018): HSRA: Hadoop-based spliced read aligner for RNA sequencing data. PLoS One, 13. doi: 10.1371/journal.pone.0201483 Go to original source... Go to PubMed...
    9. He X., Feng T., Zhang D., Zhuo R., Liu M. (2019): Identification and comprehensive analysis of the characteristics and roles of leucine-rich repeat receptor-like protein kinase (LRR-RLK) genes in Sedum alfredii Hance responding to cadmium stress. Ecotoxicology and Environmental Safety, 167: 95-106. Go to original source... Go to PubMed...
    10. Hofberger J.A., Zhou B., Tang H., Jones J.D., Schranz M.E. (2014): A novel approach for multi-domain and multi-gene family identification provides insights into evolutionary dynamics of disease resistance genes in core eudicot plants. BMC Genomics, 15. doi: 10.1186/1471-2164-15-966 Go to original source... Go to PubMed...
    11. Hok S., Allasia V., Andrio E., Naessens E., Ribes E., Panabières F., Attard A., Ris N., Clément M., Barlet X., Marco Y., Grill E., Eichmann R., Weis C., Hückelhoven R., Ammon A., Ludwig-Müller J., Voll L.M., Keller H. (2014): The receptor kinase IMPAIRED OOMYCETE SUSCEPTIBILITY1 attenuates abscisic acid responses in Arabidopsis. Plant Physiology, 166: 1506-1518. Go to original source... Go to PubMed...
    12. Huault E., Laffont C., Wen J., Mysore K.S., Ratet P., Duc G., Frugier F. (2014): Local and systemic regulation of plant root system architecture and symbiotic nodulation by a receptor-like kinase. PLoS Genetics, 10. doi: 10.1371/journal.pgen.1004891 Go to original source... Go to PubMed...
    13. Hwang S.G., Kim D.S., Jang C.S. (2011): Comparative analysis of evolutionary dynamics of genes encoding leucine-rich repeat receptor-like kinase between rice and Arabidopsis. Genetica, 139: 1023-1032. Go to original source... Go to PubMed...
    14. Kumar S., Stecher G., Tamura K. (2016): MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33: 1870-1874. Go to original source... Go to PubMed...
    15. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. (2007): Clustal W and Clustal X version 2.0. Bioinformatics, 23: 2947-2948. Go to original source... Go to PubMed...
    16. Li Z., Wang Y., Huang J., Ahsan N., Biener G., Paprocki J., Thelen J.J., Raicu V., Zhao D. (2017): Two SERK receptorlike kinases interact with ems1 to control anther cell fate determination. Plant Physiology, 173: 326-337. Go to original source... Go to PubMed...
    17. Li X., Salman A., Guo C., Yu J., Cao S., Gao X., Li W., Li H., Guo Y. (2018): Identification and characterization of LRRRLK family genes in potato reveal their involvement in peptide signaling of cell fate decisions and biotic/abiotic stress responses. Cells, 7. doi: 10.3390/cells7090120 Go to original source... Go to PubMed...
    18. Liu Z., Wu Y., Yang F., Zhang Y., Chen S., Xie Q., Tian X., Zhou J.M. (2013): BIK1 interacts with PEPRs to mediate ethylene-induced immunity. Proceedings of the National Academy of Sciences of the United States of America, 110: 6205-6210. Go to original source... Go to PubMed...
    19. Liu P.L., Xie L.L., Li P.W., Mao J.F., Liu H., Gao S.M., Shi P.H., Gong J.Q. (2016): Duplication and divergence of leucinerich repeat receptor-like protein kinase (LRR-RLK) genes in basal Angiosperm Amborella trichopoda. Frontiers in Plant Science, 7. doi: 10.3389/fpls.2016.01952 Go to original source... Go to PubMed...
    20. Liu P.L., Du L., Huang Y., Gao S.M., Yu M. (2017): Origin and diversification of leucine-rich repeat receptor-like protein kinase (LRR-RLK) genes in plants. BMC Evolutionary Biology, 17. doi: 10.1186/s12862-017-0891-5 Go to original source... Go to PubMed...
    21. Lozano-Elena F., Caño-Delgado A.I. (2019): Emerging roles of vascular brassinosteroid receptors of the BRI1-like family. Current Opinion in Plant Biology, 51: 105-113. Go to original source... Go to PubMed...
    22. Lu X., Shi H., Ou Y., Cui Y., Chang J., Peng L., Gou X., He K., Li J. (2020): RGF1-RGI1, a peptide-receptor complex, regulates Arabidopsis root meristem development via a MAPK signaling cascade. Molecular Plant, 13: 1594-1607. Go to original source... Go to PubMed...
    23. Luu D.D., Joe A., Chen Y., Parys K., Bahar O., Pruitt R., Chan L.J.G., Petzold C.J., Long K., Adamchak C., Stewart V., Belkhadir Y., Ronald P.C. (2019): Biosynthesis and secretion of the microbial sulfated peptide RaxX and binding to the rice Xa21 immune receptor. Proceedings of the National Academy of Sciences of the United States of America, 116: 8525-8534. Go to original source... Go to PubMed...
    24. Macho A.P., Zipfel C. (2014): Plant PRRs and the activation of innate immune signaling. Molecular Cell, 54: 263-272. Go to original source... Go to PubMed...
    25. Magalhães D.M., Scholte L.L., Silva N.V., Oliveira G.C., Zipfel C., Takita M.A., De Souza A.A. (2016): LRR-RLK family from two Citrus species: Genome-wide identification and evolutionary aspects. BMC Genomics, 17. doi: 10.1186/s12864-016-2930-9 Go to original source... Go to PubMed...
    26. Meng J., Yang J., Peng M., Liu X., He H. (2020): Genome-wide characterization, evolution, and expression analysis of the leucine-rich repeat receptor-like protein kinase (LRR-RLK) gene family in Medicago truncatula. Life (Basel), 10. doi: 10.3390/life10090176 Go to original source... Go to PubMed...
    27. Mishra D., Suri G.S., Kaur G., Tiwari M. (2021): Comprehensive analysis of structural, functional, and evolutionary dynamics of Leucine Rich Repeats-RLKs in Thinopyrum elongatum. International Journal of Biological Macromolecules, 183: 513-527. Go to original source... Go to PubMed...
    28. Miyazawa H., Oka-Kira E., Sato N., Takahashi H., Wu G.J., Sato S., Hayashi M., Betsuyaku S., Nakazono M., Tabata S., Harada K., Sawa S., Fukuda H., Kawaguchi M. (2010): The receptor-like kinase KLAVIER mediates systemic regulation of nodulation and non-symbiotic shoot development in Lotus japonicus. Development, 137: 4317-4325. Go to original source... Go to PubMed...
    29. Mott G.A., Thakur S., Smakowska E., Wang P.W., Belkhadir Y., Desveaux D., Guttman D.S. (2016): Genomic screens identify a new phytobacterial microbe-associated molecular pattern and the cognate Arabidopsis receptor-like kinase that mediates its immune elicitation. Genome Biology, 17. doi: 10.1186/s13059-016-0955-7 Go to original source... Go to PubMed...
    30. Pertea M., Pertea G.M., Antonescu C.M., Chang T.C., Mendell J.T., Salzberg S.L. (2015): StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nature Biotechnology, 33: 290-295. Go to original source... Go to PubMed...
    31. Robinson M.D., McCarthy D.J., Smyth G.K. (2010): edgeR: A bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics, 26: 139-140. Go to original source... Go to PubMed...
    32. Shiu S.H., Bleecker A.B. (2001): Plant receptor-like kinase gene family: Diversity, function, and signaling. Science Signaling, 2001. doi: 10.1126/stke.2001.113.re22 Go to original source... Go to PubMed...
    33. Sun X., Wang G.L. (2011): Genome-wide identification, characterization and phylogenetic analysis of the rice LRRkinases. PLoS One, 6. doi: 10.1371/journal.pone.0016079 Go to original source... Go to PubMed...
    34. Sun Y., Li L., Macho A.P., Han Z., Hu Z., Zipfel C., Zhou J.M., Chai J. (2013): Structural basis for flg22-induced activation of the Arabidopsis FLS2-BAK1 immune complex. Science, 342: 624-628. Go to original source... Go to PubMed...
    35. Sun J., Li L., Wang P., Zhang S., Wu J. (2017): Genome-wide characterization, evolution, and expression analysis of the leucine-rich repeat receptor-like protein kinase (LRR-RLK) gene family in Rosaceae genomes. BMC Genomics, 18. doi: 10.1186/s12864-017-4155-y Go to original source... Go to PubMed...
    36. Tanaka K., Choi J., Cao Y., Stacey G. (2014): Extracellular ATP acts as a damage-associated molecular pattern (DAMP) signal in plants. Frontiers in Plant Scienc, 5. doi: 10.3389/fpls.2014.00446 Go to original source... Go to PubMed...
    37. Tiwari M., Pandey V., Singh B., Yadav M., Bhatia S. (2021): Evolutionary and expression dynamics of LRR-RLKs and functional establishment of KLAVIER homolog in shoot mediated regulation of AON in chickpea symbiosis. Genomics, 113: 4313-4326. Go to original source... Go to PubMed...
    38. Wang Y., Tang H., Debarry J.D., Tan X., Li J., Wang X., Lee T.H., Jin H., Marler B., Guo H., Kissinger J.C., Paterson A.H. (2012): MCScanX: A toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Research, 40. doi: 10.1093/nar/gkr1293 Go to original source... Go to PubMed...
    39. Wang L., Albert M., Einig E., Fürst U., Krust D., Felix G. (2016): The pattern-recognition receptor CORE of Solanaceae detects bacterial cold-shock protein. Nature Plants, 2. doi: 10.1038/nplants.2016.185 Go to original source... Go to PubMed...
    40. Wang J., Liu S., Li C., Wang T., Zhang P., Chen K. (2017): PnLRR-RLK27, a novel leucine-rich repeats receptor-like protein kinase from the Antarctic moss Pohlia nutans, positively regulates salinity and oxidation-stress tolerance. PLoS One, 12. doi: 10.1371/journal.pone.0172869 Go to original source... Go to PubMed...
    41. Wang H., Chen Y., Wu X., Long Z., Sun C., Wang H., Wang S., Birch P.R.J., Tian Z. (2018): A potato Strubbelig-Receptor family member, StLRPK1, associates with StSERK3A/BAK1 and activates immunity. Journal of Experimental Botany, 69: 5573-5586. Go to original source... Go to PubMed...
    42. Wang J., Hu T., Wang W., Hu H., Wei Q., Bao C. (2019): Investigation of evolutionary and expressional relationships in the function of the leucine-rich repeat receptorlike protein kinase gene family (LRR-RLK) in the radish (Raphanus sativus L.). Scientific Reports, 9. doi: 10.1038/s41598-019-43516-9 Go to original source... Go to PubMed...
    43. Wu Y., Xun Q., Guo Y., Zhang J., Cheng K., Shi T., He K., Hou S., Gou X., Li J. (2016): Genome-wide expression pattern analyses of the arabidopsis leucine-rich repeat receptor-like kinases. Molecular Plant, 9: 289-300. Go to original source... Go to PubMed...
    44. Yan S., Ning K., Wang Z., Liu X., Zhong Y., Ding L., Zi H., Cheng Z., Li X., Shan H., Lv Q., Luo L., Liu R., Yan L., Zhou Z., Lucas W.J., Zhang X. (2020): CsIVP functions in vasculature development and downy mildew resistance in cucumber. PLoS Biology, 18. doi: 10.1371/journal.pbio.3000671 Go to original source... Go to PubMed...
    45. Yang D.L., Shi Z., Bao Y., Yan J., Yang Z., Yu H., Li Y., Gou M., Wang S., Zou B., Xu D., Ma Z., Kim J., Hua J. (2017): Calcium pumps and interacting BON1 protein modulate calcium signature, stomatal closure, and plant immunity. Plant Physiology, 175: 424-437. Go to original source... Go to PubMed...
    46. Yeh Y.H., Panzeri D., Kadota Y., Huang Y.C., Huang P.Y., Tao C.N., Roux M., Chien H.C., Chin T.C., Chu P.W., Zipfel C., Zimmerli L. (2016): The Arabidopsis malectinlike/LRR-RLK IOS1 is critical for BAK1-dependent and BAK1-independent pattern-triggered immunity. Plant Cell, 28: 1701-1721. Go to original source... Go to PubMed...
    47. Yu X., Feng B., He P., Shan L. (2017): From chaos to harmony: Responses and signaling upon microbial pattern recognition. Annual Review of Phytopathology, 55: 109-137. Go to original source... Go to PubMed...
    48. Yuan N., Rai K.M., Balasubramanian V.K., Upadhyay S.K., Luo H., Mendu V. (2018): Genome-wide identification and characterization of LRR-RLKs reveal functional conservation of the SIF subfamily in cotton (Gossypium hirsutum). BMC Plant Biololy, 18. doi: 10.1186/s12870-018-1395-1 Go to original source... Go to PubMed...
    49. Zan Y., Ji Y., Zhang Y., Yang S., Song Y., Wang J. (2013): Genome-wide identification, characterization and expression analysis of populus leucine-rich repeat receptor-like protein kinase genes. BMC Genomics, 14. doi: 10.1186/14712164-14-318 Go to original source... Go to PubMed...
    50. Zhou F., Guo Y., Qiu L.J. (2016): Genome-wide identification and evolutionary analysis of leucine-rich repeat receptorlike protein kinase genes in soybean. BMC Plant Biology, 16. doi: 10.1186/s12870-016-0744-1 Go to original source... Go to PubMed...
    51. Zhu F., Deng J., Chen H., Liu P., Zheng L., Ye Q., Li R., Brault M., Wen J., Frugier F., Dong J., Wang T. (2020): A CEP peptide receptor-like kinase regulates auxin biosynthesis and ethylene signaling to coordinate root growth and symbiotic nodulation in Medicago truncatula. Plant Cell, 32: 2855-2877. Go to original source... Go to PubMed...
    52. Zipfel C. (2008): Pattern-recognition receptors in plant innate immunity. Current Opinion in Immunology, 20: 10-16. Go to original source... Go to PubMed...
    53. Zipfel C., Kunze G., Chinchilla D., Caniard A., Jones J.D., Boller T., Felix G. (2006): Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacteriummediated transformation. Cell, 125: 749-760. Go to original source... Go to PubMed...

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