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Genome-Wide Identification and Expression Analysis of the CrRLK1L Gene Family in Apple (Malus domestica)

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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.

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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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Greeff CC, Roux MM, Mundy JJ, Petersen MM (2012) Receptor-like kinase complexes in plant innate immunity. Front Plant Sci 3:209

    PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Gusberti M, Gessler C, Broggini GA (2013) RNA-Seq analysis reveals candidate genes for ontogenic resistance in Malus-Venturia pathosystem. PLoS One 8:e78457

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Kellerhals M (2009) Introduction to apple (Malus× domestica). In: Genetics and genomics of Rosaceae. Springer, New York, pp 73–84

    Chapter  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Nissen KS, Willats WG, Malinovsky FG (2016) Understanding CrRLK1L function: cell walls and growth control. Trends Plant Sci 21:516–527

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Reed A, Mazzola M (2015) Characterization of apple replant disease-associated microbial communities over multiple growth periods using next-generation sequencing. Phytopathology 105:S4

    Article  Google Scholar 

  • Rodrigo J (2000) Spring frosts in deciduous fruit trees-morphological damage and flower hardiness. Sci Hortic 85:155–173

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Walker JC (1994) Structure and function of the receptor-like protein kinases of higher plants. Plant Mol Biol 26:1599–1609

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Zipfel C (2008) Pattern-recognition receptors in plant innate immunity. Curr Opin Immunol 20:10–16

    Article  CAS  Google Scholar 

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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).

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  1. Cunwu Zuo and Weina Zhang contributed equally to this work.

Authors and Affiliations

  1. College of Horticulture, Gansu Agricultural University, No. 1 YingmenVillage, Anning District, Lanzhou, 730070, Gansu Province, People’s Republic of China

    Cunwu Zuo, Weina Zhang, Zonghuan Ma, Mingyu Chu, Juan Mao, Zeshan An & Baihong Chen

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  1. Cunwu Zuo
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  2. Weina Zhang
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  3. Zonghuan Ma
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  4. Mingyu Chu
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  7. Baihong Chen
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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.

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Correspondence to Baihong Chen.

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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.

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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

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