Abstract
It has been reported that members of the Catharanthus roseus receptor-like kinase1-like kinase (CrRLK1L) gene family detect cell wall integrity, cell-to-cell communication, and biotic and abiotic stress. We performed a comprehensive study including the genome-wide identification, characterization, and gene expression analysis of CrRLK1Ls in apple (Malus domestica). Sixty-seven M. domestica CrRLK1Ls (MdCrRLK1Ls) were identified based on their domain structure. Molecular weight and pI ranged from 52.36–141 kDa and 5.05–8.9, respectively. They were distributed across 16 of the 18 chromosomes and classified into five phylogenetic branches. Exon-intron structural analysis indicated a wide range of exon numbers. Collinearity analysis showed that both segmental-and tandem-duplication contributed to the expansion of this family. Cis-elements in the MdCrRLK1L promoter region responded mainly to light, circadian rhythm, phytohormones, and biotic or abiotic stress. Many members exhibited tissue-specific expression patterns and differentially expressed under biotic stresses, which may contribute to the different functional roles of MdCrRLK1Ls under physiological stress and/or pathological conditions. This study provides new insights into the CrRLK1Ls in Malus spp.
Similar content being viewed by others
Abbreviations
- RLK:
-
receptor-like kinase
- CrRLK1L :
-
Catharanthus roseus receptor-like kinase1-like kinase
- MdCrRLK1L :
-
Malus domestica CrRLK1L
- GDR:
-
Genome database of Rosaceae species
- GEF:
-
guanine nucleotide exchange factor
- RAC/ROP:
-
GEF-regulated Rho GTPase
- ROS:
-
reactive oxygen species
- RT-qPCR:
-
quantitative real-time PCR
- FLS2:
-
Flagellin sensing2
- EFR:
-
Ef-Tu receptor
- CERK1:
-
chitin elicitor receptor kinase 1
- PRR:
-
pattern recognition receptor
- PTI:
-
pattern-triggered immunity
References
Bassett CL, Baldo AM, Moore JT, Jenkins RM, Soffe DS, Wisniewski ME, Norelli JL, Farrell RE (2014) Genes responding to water deficit in apple (Malus× domestica Borkh.) roots. BMC Plant Biol 14:1–12
Boisson-Dernier A, Kessler SA, Grossniklaus U (2011) The walls have ears: the role of plant CrRLK1Ls in sensing and transducing extracellular signals. J Exp Bot 62:1581–1591
Byers RE, Marini RP (1994) Influence of blossom and fruit thinning on peach flower bud tolerance to an early spring freeze. HortSci 29:146–148
Celton JM, Gaillard S, Bruneau M, Pelletier S, Aubourg S, Martin-Magniette ML, Navarro L, Laurens F, Renou JP (2014) Widespread anti-sense transcription in apple is correlated with siRNA production and indicates a large potential for transcriptional and/or post-transcriptional control. New Phytol 203:287–299
Chen J, Yu F, Liu Y, Du C, Li X, Zhu S, Wang X, Rodriguez PL, Liu D, Chen L, Luan S (2016) FERONIA interacts with ABI2-type phosphatases to facilitate signaling cross-talk between abscisic acid and RALF peptide in Arabidopsis. Proc Natl Acad Sci U S A 113:E5519–E5527
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
Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer EL, Tate J, Punta M (2014) Pfam: the protein families database. Nucleic Acids Res 42:D222–D230
Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 9:436–442
Gallai N, Salles JM, Settele J, Vaissière BE (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol Econ 68:810–821
Giorno F, Guerriero G, Baric S, Mariani C (2012) Heat shock transcriptional factors in Malus domestica: identification, classification and expression analysis. BMC Genomics 13(1):639
Greeff CC, Roux MM, Mundy JJ, Petersen MM (2012) Receptor-like kinase complexes in plant innate immunity. Front Plant Sci 3:209
Guo H, Ye H, Li L, Yin Y (2009) A family of receptor-like kinases are regulated by BES1 and involved in plant growth in Arabidopsis thaliana. Plant Signal Behav 4:784–786
Gusberti M, Gessler C, Broggini GA (2013) RNA-Seq analysis reveals candidate genes for ontogenic resistance in Malus-Venturia pathosystem. PLoS One 8:e78457
Han YF, Yang Q, Zhang SW, Sun DY, Sun Y (2011) Receptor like kinase CrRLK1-L subfamily: novel motifs in extracellular domain and biological functions in plants. Prog Biochem Biophys 38:891–899
Hanks SK, Hunter T (1995) Protein kinases 6. The eukaryotic protein kinase super family: kinase (catalytic) domain structure and classification. FASEB J 9:576–596
Haruta M, Sabat G, Stecker K, Minkoff BB, Sussman MR (2014) A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science 343:408–411
Hématy K, Sado PE, Van Tuinen A, Rochange S, Desnos T, Balzergue S, Pelletier S, Renou JP, Höfte H (2007) A receptor-like kinase mediates the response of Arabidopsis cells to the inhibition of cellulose synthesis. Curr Biol 17:922–931
Hu R, Qi G, Kong Y, Kong D, Gao Q, Zhou G (2010) Comprehensive analysis of NAC domain transcription factor gene family in Populus trichocarpa. BMC Plant Biol 10:145
Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2014) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297
Huck N, Moore JM, Federer M, Grossniklaus U (2003) The Arabidopsis mutant feronia disrupts the female gametophytic control of pollen tube reception. Development 130:2149–2159
Kanaoka MM, Torii KU (2010) FERONIA as an upstream receptor kinase for polar cell growth in plants. Proc Natl Acad Sci U S A 107:17461–17462
Kellerhals M (2009) Introduction to apple (Malus× domestica). In: Genetics and genomics of Rosaceae. Springer, New York, pp 73–84
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
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948
Lecharny A, Boudet N, Gy I, Aubourg S, Kreis M (2003) Introns in, introns out in plant gene families: a genomic approach of the dynamics of gene structure. J Struct Funct Genom 3:111–116
Lehti-Shiu MD, Zou C, Hanada K, Shiu SH (2009) Evolutionary history and stress regulation of plant receptor-like kinase/pelle genes. Plant Physiol 150:12–26
Lehti-Shiu MD, Zou C, Shiu SH (2012) Origin, diversity, expansion history, and functional evolution of the plant receptor-like kinase/pelle family. In: Receptor-Like Kinases in Plants. Springer, Berlin Heidelberg, pp 1–22
Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327
Li Z, Yin Z, Fan Y, Xu M, Kang Z, Huang L (2015) Candidate effector proteins of the necrotrophic apple canker pathogen valsa mali can suppress bax-induced PCD. Front Plant Sci 6:579
Lindner H, Muller LM, Boisson-Dernier A, Grossniklaus U (2012) CrRLK1L receptor-like kinases: not just another brick in the wall. Curr Opin Plant Biol 15:659–669
Nguyen QN, Lee YS, Cho LH, Jeong HJ, An G, Jung KH (2015) Genome-wide identification and analysis of Catharanthus roseus RLK1-like kinases in rice. Planta 241:603–613
Nibau C, Cheung A (2011) New insights into the functional roles of CrRLKs in the control of plant cell growth and development. Plant Signal Behav 6:655–659
Nissen KS, Willats WG, Malinovsky FG (2016) Understanding CrRLK1L function: cell walls and growth control. Trends Plant Sci 21:516–527
Niu E, Cai C, Zheng Y, Shang X, Fang L, Guo W (2016) Genome-wide analysis of CrRLK1L gene family in Gossypium and identification of candidate CrRLK1L genes related to fiber development. Mol Gen Genomics 291:1137–1154
Rajaraman J, Douchkov D, Hensel G, Stefanato FL, Gordon A, Ereful N, Caldararu OF, Petrescu A, Kumlehn J, Boyd LA, Schweizer P (2016) An LRR/malectin receptor-like kinase mediates resistance to non-adapted and adapted powdery mildew fungi in barley and wheat. Front Plant Sci 7:1836
Reed A, Mazzola M (2015) Characterization of apple replant disease-associated microbial communities over multiple growth periods using next-generation sequencing. Phytopathology 105:S4
Rodrigo J (2000) Spring frosts in deciduous fruit trees-morphological damage and flower hardiness. Sci Hortic 85:155–173
Schultz J, Milpetz F, Bork P, Ponting CP (1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci U S A 95:5857–5864
Schulze-Muth P, Irmler S, Schröder G, Schröder J (1996) Novel type of receptor-like protein kinase from a higher plant (Catharanthusroseus) cDNA, gene, intramolecular autophosphorylation, and identification of a threonine important for auto- and substrate phosphorylation. J Biol Chem 271:26684–26689
Shin S, Zheng P, Fazio G, Mazzola M, Main D, Zhu Y (2016) Transcriptome changes specifically associated with apple (Malus domestica) root defense response during Pythium ultimum infection. Physiol Mol Plant Pathol 94:16–26
Shiu SH, Karlowski WM, Pan R, Tzeng YH, Mayer KF, Li WH (2004) Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16:1220–1234
Stegmann M, Monaghan J, Smakowska-Luzan E, Rovenich H, Lehner A, Holton N, Belkhadir Y, Zipfel C (2017) The receptor kinase FER is a RALF-regulated scaffold controlling plant immune signaling. Science 355:287–289
Stracke S, Kistner C, Yoshida S, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Szczyglowski K, Parniske M (2002) A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417:959–962
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D, Salvi S, Pindo M, Baldi P, Castelletti S, Cavaiuolo M, Coppola G, Costa F, Cova V, Ri AD, Goremykin V, Komjanc M, Longhi S, Magnago P, Malacarne G, Malnoy M, Micheletti D, Moretto M, Perazzolli M, Si-Ammour A, Vezzulli S, Zini E, Eldredge G, Fitzgerald LM, Gutin N, Lanchbury J, Macalma T, Mitchell JT, Reid J, Wardell B, Kodira C, Chen Z, Desany B, Niazi F, Palmer M, Koepke T, Jiwan D, Schaeffer S, Krishnan V, Wu C, Chu VT, King ST, Vick J, Tao Q, Mraz A, Stormo A, Stormo K, Bogden R, Ederle D, Stella A, Vecchietti A, Kater MM, Masiero S, Lasserre P, Lespinasse Y, Allan AC, Bus V, Chagné D, Crowhurst RN, Gleave AP, Lavezzo E, Fawcett JA, Proost S, Rouzé P, Sterck L, Toppo S, Lazzari B, Hellens RP, Durel C, Gutin A, Bumgarner RE, Gardiner SE, Skolnick M, Egholm M, Peer YV, Salamin F (2010) The genome of the domesticated apple (Malus [times] domestica Borkh.). Nat Genet 42:833–839
Walker JC (1994) Structure and function of the receptor-like protein kinases of higher plants. Plant Mol Biol 26:1599–1609
Walker JC, Zhang R (1990) Relationship of a putative receptor protein kinase from maize to the S-locus glycoproteins of Brassica. Nature 345:743–746
Wang G, Ellendorff U, Kemp B, Mansfield JW, Forsyth A, Mitchell K, Bastas K, Liu C, Woods-Tör A, Zipfel C, de Wit PJ, Jones JD, Tör M, Thomma BP (2008) A genome-wide functional investigation into the roles of receptor-like proteins in Arabidopsis. Plant Physiol 147:503–517
Wang Y, Tang H, Debarry JD, Tan X, Li J, Wang X, Lee TH, Jin H, Marler B, Guo H, Kissinger JC, Paterson AH (2012) MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res 40:e49
Wang S, Hu T, Wang Y, Luo Y, Michailides TJ, Cao K (2016) New understanding on infection processes of Valsa canker of apple in China. Eur J Plant Pathol 146:531–540
Wu R, Wang Y, Wu T, Xu X, Han Z (2017) MdMYB4, an R2R3-type MYB transcription factor, plays a crucial role in cold and salt stress in apple. J Am Soc Hortic Sci 142:209–216
Yamaguchi H, Matsushita M, Nairn AC, Kuriyan J (2001) Crystal structure of the atypical protein kinase domain of a TRP channel with phosphotransferase activity. Mol Cell 7:1047–1057
Yeh YH, Panzeri D, Kadota Y, Huang YC, Huang PY, Tao CN, Roux M, Chien HC, Chin TC, Chu PW, Zipfel C, Zimmerli L (2016) The Arabidopsis malectin-like/LRR-RLK IOS1 is critical for BAK1-dependent and BAK1-independent pattern-triggered immunity. Plant Cell 28:1701–1721
Yin Z, Ke X, Kang Z, Huang L (2016) Apple resistance responses against valsa mali, revealed by transcriptomics analyses. Physiol Mol Plant 93:85–92
Yu F, Qian L, Nibau C, Duan Q, Kita D, Levasseur K, Li X, Lu C, Li H, Hou C, Li L, Buchanan BB, Chen L, Cheung AY, Li D, Luan S (2012) FERONIA receptor kinase pathway suppresses abscisic acid signaling in Arabidopsis by activating ABI2 phosphatase. Proc Natl Acad Sci U S A 109:14693–14698
Zipfel C (2008) Pattern-recognition receptors in plant innate immunity. Curr Opin Immunol 20:10–16
Funding
This work was supported by the horticultural innovation fund of Gansu Agricultural University (GAU-XKJS-2018-217), the National Natural Science Foundation of China (31860549; 31501728), the Science and Technology Major Project of Gansu Province (18ZD2NA006), and the Fund for higher education of Gansu province (2018B-034).
Author information
Authors and Affiliations
Contributions
ZC, CB, and ZW conceived and designed the study; ZC, MZ, CM, MJ, and AZ performed the experiments, analyzed the data, and wrote the manuscript. All the authors agreed on the content of this manuscript.
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no conflict of interest.
Data Archiving Statement
All identified amino acid and/or CDS of MdCrRLK1L gene sequences were deposited into the GDR (https://www.rosaceae.org/species/malus/all) and/or NCBI database (http://www.ncbi.nlm.nih.gov/). The accession numbers are listed in Table 1.
Electronic supplementary material
Supplementary Table 1
(DOCX 13 kb)
Supplementary Table 2
(DOCX 13 kb)
Supplementary Table 3
(DOCX 14 kb)
Supplementary Table 4
(DOCX 24 kb)
Supplementary Table 5
(DOCX 24 kb)
Supplementary Table 6
(XLSX 15 kb)
Rights and permissions
About this article
Cite this article
Zuo, C., Zhang, W., Ma, Z. et al. Genome-Wide Identification and Expression Analysis of the CrRLK1L Gene Family in Apple (Malus domestica). Plant Mol Biol Rep 36, 844–857 (2018). https://doi.org/10.1007/s11105-018-1125-8
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11105-018-1125-8