Identification and Characterization of LRR-RLK Family Genes in Potato Reveal Their Involvement in Peptide Signaling of Cell Fate Decisions and Biotic/Abiotic Stress Responses
Abstract
:1. Introduction
2. Materials and Methods
2.1. Identification and Phylogenetic Analysis
2.2. Motif and Gene Structure Analysis
2.3. Chromosomal Localization Analysis
2.4. Expression Profiling of StLRR-RLKs
2.5. Potato Materials
2.6. RNA Extraction and qRT-PCR
2.7. Bimolecular Fluorescence Complementation Assays
3. Results
3.1. Identification and Phylogenetic Analysis of Potato LRR-RLKs
3.2. Conserved and Functional Motifs
3.3. Exon–Intron Organization
3.4. Chromosome Localization and Duplication Analysis
3.5. The Expression Pattern in Tested Tissues
3.6. Expression Profiling of StLRR-RLK Genes during Abiotic and Biotic Stresses
3.7. Validation of Expression Patterns by qRT-PCR
3.8. Bimolecular Fluorescence Complementation Assays
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Gish, L.A.; Clark, S.E. The RLK/Pelle family of kinases. Plant J. 2011, 66, 117–127. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shiu, S.H.; Bleecker, A.B. Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc. Natl. Acad. Sci. USA 2001, 98, 10763–10768. [Google Scholar] [CrossRef] [PubMed]
- Shiu, S.H.; Karlowski, W.M.; Pan, R.; Tzeng, Y.H.; Mayer, K.F.; Li, W.H. Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 2004, 16, 1220–1234. [Google Scholar] [CrossRef] [PubMed]
- Clark, S.E.; Williams, R.W.; Meyerowitz, E.M. The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 1997, 89, 575–585. [Google Scholar] [CrossRef]
- Clark, S.E.; Running, M.P.; Meyerowitz, E.M. CLAVATA1, a regulator of meristem and flower development in Arabidopsis. Development 1993, 119, 397–418. [Google Scholar] [PubMed]
- Schoof, H.; Lenhard, M.; Haecker, A.; Mayer, K.F.; Jürgens, G.; Laux, T. The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 2000, 100, 635–644. [Google Scholar] [CrossRef]
- Clark, S.E. Cell signalling at the shoot meristem. Nat. Rev. Mol. Cell Biol. 2001, 2, 276. [Google Scholar] [CrossRef] [PubMed]
- DeYoung, B.J.; Bickle, K.L.; Schrage, K.J.; Muskett, P.; Patel, K.; Clark, S.E. The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis. Plant J. 2006, 45, 1–16. [Google Scholar] [CrossRef] [PubMed]
- Guo, Y.; Han, L.; Hymes, M.; Denver, R.; Clark, S.E. CLAVATA2 forms a distinct CLE-binding receptor complex regulating Arabidopsis stem cell specification. Plant J. 2010, 63, 889–900. [Google Scholar] [CrossRef] [PubMed]
- Hu, C.; Zhu, Y.; Cui, Y.; Cheng, K.; Liang, W.; Wei, Z.; Zhu, M.; Yin, H.; Zeng, L.; Xiao, Y. A group of receptor kinases are essential for CLAVATA signalling to maintain stem cell homeostasis. Nat. Plants 2018, 4, 205. [Google Scholar] [CrossRef] [PubMed]
- Hirakawa, Y.; Kondo, Y.; Fukuda, H. TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in Arabidopsis. Plant Cell 2010, 22, 2618–2629. [Google Scholar] [CrossRef] [PubMed]
- Zhang, H.; Lin, X.; Han, Z.; Qu, L.J.; Chai, J. Crystal structure of PXY-TDIF complex reveals a conserved recognition mechanism among CLE peptide-receptor pairs. Cell Res. 2016, 26, 543. [Google Scholar] [CrossRef] [PubMed]
- Kondo, Y.; Fukuda, H. The TDIF signaling network. Curr. Opin. Plant Biol. 2015, 28, 106–110. [Google Scholar] [CrossRef] [PubMed]
- Fisher, K.; Turner, S. PXY, a receptor-like kinase essential for maintaining polarity during plant vascular-tissue development. Curr. Biol. 2007, 17, 1061–1066. [Google Scholar] [CrossRef] [PubMed]
- Stenvik, G.E.; Tandstad, N.M.; Guo, Y.; Shi, C.-L.; Kristiansen, W.; Holmgren, A.; Clark, S.E.; Aalen, R.B.; Butenko, M.A. The EPIP peptide of INFLORESCENCE DEFICIENT IN ABSCISSION is sufficient to induce abscission in Arabidopsis through the receptor-like kinases HAESA and HAESA-LIKE2. Plant Cell 2008, 20, 1805–1817. [Google Scholar] [CrossRef] [PubMed]
- Tabata, R.; Sumida, K.; Yoshii, T.; Ohyama, K.; Shinohara, H.; Matsubayashi, Y. Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling. Science 2014, 346, 343–346. [Google Scholar] [CrossRef] [PubMed]
- Song, W.; Liu, L.; Wang, J.; Wu, Z.; Zhang, H.; Tang, J.; Lin, G.; Wang, Y.; Wen, X.; Li, W. Signature motif-guided identification of receptors for peptide hormones essential for root meristem growth. Cell Res. 2016, 26, 674. [Google Scholar] [CrossRef] [PubMed]
- Matsuzaki, Y.; Ogawa-Ohnishi, M.; Mori, A.; Matsubayashi, Y. Secreted peptide signals required for maintenance of root stem cell niche in Arabidopsis. Science 2010, 329, 1065–1067. [Google Scholar] [CrossRef] [PubMed]
- Lee, J.S.; Hnilova, M.; Maes, M.; Lin, Y.C.L.; Putarjunan, A.; Han, S.-K.; Avila, J.; Torii, K.U. Competitive binding of antagonistic peptides fine-tunes stomatal patterning. Nature 2015, 522, 439. [Google Scholar] [CrossRef] [PubMed]
- He, Z.; Wang, Z.Y.; Li, J.; Zhu, Q.; Lamb, C.; Ronald, P.; Chory, J. Perception of brassinosteroids by the extracellular domain of the receptor kinase BRI1. Science 2000, 288, 2360–2363. [Google Scholar] [CrossRef] [PubMed]
- Kinoshita, T.; Cano-Delgado, A.; Seto, H.; Hiranuma, S.; Fujioka, S.; Yoshida, S.; Chory, J. Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1. Nature 2005, 433, 167. [Google Scholar] [CrossRef] [PubMed]
- Huffaker, A.; Pearce, G.; Ryan, C.A. An endogenous peptide signal in Arabidopsis activates components of the innate immune response. Proc. Natl. Acad. Sci. USA 2006, 103, 10098–10103. [Google Scholar] [CrossRef] [PubMed]
- Yamaguchi, Y.; Huffaker, A.; Bryan, A.C.; Tax, F.E.; Ryan, C.A. PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis. Plant Cell 2010, 22, 508–522. [Google Scholar] [CrossRef] [PubMed]
- Chinchilla, D.; Bauer, Z.; Regenass, M.; Boller, T.; Felix, G. The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 2006, 18, 465–476. [Google Scholar] [CrossRef] [PubMed]
- Sun, Y.; Li, L.; Macho, A.P.; Han, Z.; Hu, Z.; Zipfel, C.; Zhou, J.M.; Chai, J. Structural basis for flg22-induced activation of the Arabidopsis FLS2-BAK1 immune complex. Science 2013, 342, 624–628. [Google Scholar] [CrossRef] [PubMed]
- Yuan, N.; Yuan, S.; Li, Z.; Zhou, M.; Wu, P.; Hu, Q.; Wang, L.; Mendu, V.; Luo, H. STRESS INDUCED FACTOR 2, a leucine-rich repeat kinase regulates basal plant pathogen defense. Plant Physiol. 2018, 176, 3062–3080. [Google Scholar] [CrossRef] [PubMed]
- Osakabe, Y.; Maruyama, K.; Seki, M.; Satou, M.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Leucine-rich repeat receptor-like kinase1 is a key membrane-bound regulator of abscisic acid early signaling in Arabidopsis. Plant Cell 2005, 17, 1105–1119. [Google Scholar] [CrossRef] [PubMed]
- Osakabe, Y.; Mizuno, S.; Tanaka, H.; Maruyama, K.; Osakabe, K.; Todaka, D.; Fujita, Y.; Kobayashi, M.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Overproduction of the membrane-bound receptor-like protein kinase1, RPK1, enhances abiotic stress tolerance in Arabidopsis. J. Biol. Chem. 2010, 285, 9190–9201. [Google Scholar] [CrossRef] [PubMed]
- Lee, I.C.; Hong, S.W.; Whang, S.S.; Lim, P.O.; Nam, H.G.; Koo, J.C. Age-dependent action of an ABA-inducible receptor kinase, RPK1, as a positive regulator of senescence in Arabidopsis leaves. Plant Cell Physiol. 2011, 52, 651–662. [Google Scholar] [CrossRef] [PubMed]
- Law, Y.S.; Gudimella, R.; Song, B.K.; Ratnam, W.; Harikrishna, J.A. Molecular characterization and comparative sequence analysis of defense-related gene, oryza rufipogon receptor-like protein kinase 1. Int. J. Mol. Sci. 2012, 13, 9343–9362. [Google Scholar] [CrossRef] [PubMed]
- Sakamoto, T.; Deguchi, M.; Brustolini, O.J.; Santos, A.A.; Silva, F.F.; Fontes, E.P. The tomato RLK superfamily: Phylogeny and functional predictions about the role of the LRRII-RLK subfamily in antiviral defense. BMC Plant Biol. 2012, 12, 229. [Google Scholar] [CrossRef] [PubMed]
- Wei, Z.; Wang, J.; Yang, S.; Song, Y. Identification and expression analysis of the LRR-RLK gene family in tomato (Solanum lycopersicum) Heinz 1706. Genome 2015, 58, 121–134. [Google Scholar] [CrossRef] [PubMed]
- Zan, Y.; Ji, Y.; Zhang, Y.; Yang, S.; Song, Y.; Wang, J. Genome-wide identification, characterization and expression analysis of populus leucine-rich repeat receptor-like protein kinase genes. BMC Genom. 2013, 14, 318. [Google Scholar] [CrossRef] [PubMed]
- Magalhães, D.M.; Scholte, L.L.; Silva, N.V.; Oliveira, G.C.; Zipfel, C.; Takita, M.A.; De Souza, A.A. LRR-RLK family from two Citrus species: Genome-wide identification and evolutionary aspects. BMC Genom. 2016, 17, 623. [Google Scholar] [CrossRef] [PubMed]
- Liu, S.; Zhang, C.; Chao, N.; Lu, J.; Zhang, Y. Cloning, Characterization, and Functional Investigation of VaHAESA from Vitis amurensis Inoculated with Plasmopara viticola. Int. J. Mol. Sci. 2018, 19, 1204. [Google Scholar] [CrossRef] [PubMed]
- Sun, J.; Li, L.; Wang, P.; Zhang, S.; Wu, J. Genome-wide characterization, evolution, and expression analysis of the leucine-rich repeat receptor-like protein kinase (LRR-RLK) gene family in Rosaceae genomes. BMC Genom. 2017, 18, 763. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Tang, H.; DeBarry, J.D.; Tan, X.; Li, J.; Wang, X.; Lee, T.H.; Jin, H.; Marler, B.; Guo, H. MCScanX: A toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 2012, 40, e49. [Google Scholar] [CrossRef] [PubMed]
- Cao, Y.; Meng, D.; Chen, Y.; Abdullah, M.; Jin, Q.; Lin, Y.; Cai, Y. Comparative and Expression Analysis of Ubiquitin Conjugating Domain-Containing Genes in Two Pyrus Species. Cells 2018, 7, 77. [Google Scholar] [CrossRef] [PubMed]
- Krzywinski, M.I.; Schein, J.E.; Birol, I.; Connors, J.; Gascoyne, R.; Horsman, D.; Jones, S.J.; Marra, M.A. Circos: An information aesthetic for comparative genomics. Genome Res. 2009, 19, 1639–1945. [Google Scholar] [CrossRef] [PubMed]
- Consortium, P.G.S. Genome sequence and analysis of the tuber crop potato. Nature 2011, 475, 189. [Google Scholar] [CrossRef]
- Nicot, N.; Hausman, J.F.; Hoffmann, L.; Evers, D. Housekeeping gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress. J. Exp. Bot. 2005, 56, 2907–2914. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, X.; Hamyat, M.; Liu, C.; Salman, A.; Gao, X.; Guo, C.; Wang, Y.; Guo, Y. Identification and Characterization of the WOX Family Genes in Five Solanaceae Species Reveal Their Conserved Roles in Peptide Signaling. Genes 2018, 9, 260. [Google Scholar] [CrossRef] [PubMed]
- Karve, R.; Liu, W.; Willet, S.G.; Torii, K.U.; Shpak, E.D. The presence of multiple introns is essential for ERECTA expression in Arabidopsis. RNA 2011, 17, 1907–1921. [Google Scholar] [CrossRef] [PubMed]
Subfamily | Gene Num. | PI | MW (kDa) | Amino Acid Length | SP (%) | Arabidopsis Best Hits |
---|---|---|---|---|---|---|
I | 9 | 5.48–9.18 | 59.6–87.0 | 533–785 | 77.8 | MRH1 |
II | 4 | 6.14–8.87 | 61.6–105.4 | 561–959 | 100 | |
III | 3 | 5.88–8.12 | 74.0–75.4 | 678–686 | 100 | |
IV | 5 | 5.62–6.26 | 75.0–80.8 | 692–738 | 80 | SRF1-8, SCM |
V | 4 | 6.26–9.35 | 76.4–105.3 | 682–946 | 100 | |
VI | 41 | 5.69–9.30 | 63.9–122.0 | 565–1127 | 75.6 | RUL1, LRR1, RLK902, RKL1, PRK2A, TMKL1 |
VII | 3 | 5.36–6.44 | 95.8–107.4 | 882–984 | 33.3 | |
VIII | 15 | 5.2–8.9 | 41.3–137.8 | 369–1272 | 66.7 | BRL1, BRL3, BRI1, PSRK1, PSKR2, BIR1 |
IX-a | 20 | 5.14–8.21 | 99.6–133.3 | 919–1230 | 80 | CLV1, BAM1-3, PXY, PXL1, RGFR1-5 |
IX-b | 16 | 5.02–8.99 | 60.6–114.6 | 542–1032 | 87.5 | HAE, HSL1-2, CEPR1-2, RLK7 |
IX-c | 8 | 5.12–9.37 | 70.2–138.1 | 625–1255 | 100 | PEPR1-2, GSO1, ERECTA, ERL1-2 |
IX-d | 10 | 5.18–9.03 | 88.7–141.0 | 804–1283 | 70 | |
X | 3 | 5.43–6.87 | 67.0–121.7 | 601–1126 | 66.7 | FEI1, FEI2 |
XI | 60 | 5.11–8.83 | 33.8–222.9 | 303–2007 | 41.7 | |
XII | 10 | 5.38–6.64 | 10.4–121.8 | 921–1106 | 90 | |
XIII | 16 | 5.43–8.4 | 57.6–113.3 | 518–1027 | 62.5 | SERK1-5, SARK, NIK1-3 |
XIV | 10 | 5.76–8.75 | 57.4–106.0 | 518–964 | 70 | SIF1-4, SIRK |
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Li, X.; Ahmad, S.; Guo, C.; Yu, J.; Cao, S.; Gao, X.; Li, W.; Li, H.; Guo, Y. Identification and Characterization of LRR-RLK Family Genes in Potato Reveal Their Involvement in Peptide Signaling of Cell Fate Decisions and Biotic/Abiotic Stress Responses. Cells 2018, 7, 120. https://doi.org/10.3390/cells7090120
Li X, Ahmad S, Guo C, Yu J, Cao S, Gao X, Li W, Li H, Guo Y. Identification and Characterization of LRR-RLK Family Genes in Potato Reveal Their Involvement in Peptide Signaling of Cell Fate Decisions and Biotic/Abiotic Stress Responses. Cells. 2018; 7(9):120. https://doi.org/10.3390/cells7090120
Chicago/Turabian StyleLi, Xiaoxu, Salman Ahmad, Cun Guo, Jing Yu, Songxiao Cao, Xiaoming Gao, Wei Li, Hong Li, and Yongfeng Guo. 2018. "Identification and Characterization of LRR-RLK Family Genes in Potato Reveal Their Involvement in Peptide Signaling of Cell Fate Decisions and Biotic/Abiotic Stress Responses" Cells 7, no. 9: 120. https://doi.org/10.3390/cells7090120