Abstract
Cysteine-rich receptor-like kinases (CRKs) took crucial roles in plant cell growth and development, as well as environmental adaption. Apple (Malus domestica) had been considered a staple fruit crop and a model of woody plants. In this study, the annotation, evolution, and duplication of the CRK gene family members in apple (MdCRK) were characterized. Besides, we also investigated the expressional patterns of MdCRKs in various tissue types and response to signals from Alternaria alternate apple pathotype (AaAP), Penicillium expansum (Pe), and Valsa mali (Vm). A total of 36 MdCRKs were annotated. The phylogenetic analysis of CRKs among apple, Arabidopsis thaliana, rice (Oryza sativa), cotton (Gossypium hirsutum), banana (Musa acuminata), and tomato (Solanum lycopersicum) revealed the distinct evolutionary characteristics in plants. Based on gene duplication analysis, seven tandem gene clusters containing 24 members and ten segmental gene pairs were found from MdCRKs. A large number segmental gene pairs were identified from CRKs between apple and cotton. Abscisic acid (ABA) and methyl jasmonate (MeJA)–responsive cis-elements were discovered from the promoter region of most MdCRKs. MdCRKs showed distinct tissue and developmental expression patterns. Most members displayed distinct expression patterns among various tissue types. Six members were differentially expressed in response to signals from at least two pathogenic fungi. Our study provides valuable information for further studies on the evolution and functional investigation on disease resistance of CRKs.
Similar content being viewed by others
Abbreviations
- CRK:
-
cysteine-rich receptor-like kinase
- AaAP:
-
Alternaria alternate apple pathotype
- Pe :
-
Penicillium expansum
- Vm :
-
Valsa mali
- ABA:
-
abscisic acid
- MeJA:
-
methyl jasmonate
- RLK:
-
receptor-like kinase
- ECD:
-
extracellular domain
- KD:
-
kinase domain
- LRR:
-
leucine-rich repeats
- TM:
-
transmembrane
References
Abe K, Iwanami H, Kotoda N, Moriya S, Takahashi S (2010) Evaluation of apple genotypes and Malus species for resistance to Alternaria blotch caused by Alternaria alternata apple pathotype using detached-leaf method. Plant Breed 129:208–218
Acharya BR, Raina S, Maqbool SB, Jagadeeswaran G, Mosher S, Appel HM, Schultz JC, Klessig DF, Raina R (2010) Overexpression of CRK13, an Arabidopsis cysteine-rich receptor-like kinase, results in enhanced resistance to Pseudomonas syringae. Plant J 50:488–499
Ballester AR, Norelli J, Burchard E, Abdelfattah A, Levin E, Gonzálezcandelas L, Droby S, Wisniewski M (2017) Transcriptomic response of resistant (pi613981-Malus sieversii) and susceptible (“royal gala”) genotypes of apple to blue mold (Penicillium expansum) infection. Front Plant Sci 8:1981
Bari R, Jones JDG (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488
Biggs AR, Turechek WW, Gottwald TR (2008) Analysis of fire blight shoot infection epidemics on apple. Plant Dis 92:1349–1356
Bourdais G, Burdiak P, Gauthier A, Nitsch L, Salojärvi J, Rayapuram C, Idänheimo N, Hunter K, Kimura S, Merilo E, Vaattovaara A, Oracz K, Kaufholdt D, Pallon A, Anggoro DT, Glów D, Lowe J, Zhou J, Mohammadi O, Puukko T, Albert A, Lang H, Ernst D, Kollist H, Brosché M, Durner J, Borst JW, Collinge DB, Karpiński S, Lyngkjær SR, Wrzaczek M, Vaattovaara A (2015) Large-scale phenomics identifies primary and fine-tuning roles for CRKs in responses related to oxidative stress. PLoS Genet 11:e1005373
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 iscorrelated with siRNA production and indicates a large potentialfor transcriptional and/or post-transcriptional control. New Phytol 203:287–299
Chen Z (2001) A superfamily of proteins with novel cysteine-rich repeats. Plant Physiol 126:473–476
Daccord N, Celton JM, Linsmith G (2017) High-quality de novo assembly of the apple genome and methylome dynamics of early fruit development. Nat Genet 49:1099–1106
Derksen H, Rampitsch C, Daayf F (2013) Signaling cross-talk in plant disease resistance. Plant Sci 207:79–87
Dezhsetan S (2017) Genome scanning for identification and mapping of receptor-like kinase (RLK) gene superfamily in Solanum tuberosum. Physiol Mol Biol Plants 23:1–11
Fischer C (2000) Multiple resistant apple cultivars and consequences for apple breeding in the future. Acta Hort 538:229–234
Fischer I, Dievart A, Droc G, Dufayard JF, Chantret N (2016) Evolutionary dynamics of the leucine-rich repeats receptor-like kinase (LRR-RLK) subfamily in angiosperms. Plant Physiol 170:1595–1610
Freeling M (2009) Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition. Annu Rev Plant Biol 60:433–453
Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227
Larkan NJ, Raman H, Lydiate DJ, Robinson SJ, Yu F, Barbulescu DM, Raman R, Luckett DJ, Burton W, Wratten N, Salisbury PA, Rimmer SR, Borhan MH (2016) Multi-environment qtl studies suggest a role for cysteine-rich protein kinase genes in quantitative resistance to blackleg disease in Brassica napus. BMC Plant Biol 16:183
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
Lee DS, Kim YC, Kwon SJ, Ryu CM, Park OK (2017) The arabidopsis cysteine-rich receptor-like kinase CRK36 regulates immunity through interaction with the cytoplasmic kinase BIK1. Front Plant Sci 8:1856
Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Peer YVD, Rouze P, Rombauts S (2002) Plantcare, a database of plant cis-acting regulatory elements and a portal to tools for in silico0020analysis of promoter sequences. Nucleic Acids Res 30:325–327
Liu Y, Lan J, Li Q, Zhang Y, Wang C, Dai H (2017) Rapid location of Glomerella leaf spot resistance gene locus in apple by whole genome re-sequencing. Mol Breed 37:96
Lu K, Liang S, Wu Z, Bi C, Yu YT, Wang XF, Zhang DP (2016) Overexpression of an arabidopsis cysteine-rich receptor-like protein kinase, crk5, enhances abscisic acid sensitivity and confers drought tolerance. J Exp Bot 67:5009–5027
Matsubayashi Y (2003) Ligand-receptor pairs in plant peptidesignaling. J Cell Sci 116:3863–3870
Mazzola M, Manici L (2012) Apple replant disease: role of microbial ecology in cause and control. Annu Rev Phytopathol 50:45–65
Mengiste T (2012) Plant immunity to necrotrophs. Annu Rev Phytopathol 50:267
Pereira-Lorenzo SFM, Ramos-Cabrer AM, Castro I (2018) Apple (Malus spp.) Breeding: Present and Future. In: Al-Khayri J, Jain S, Johnson D (eds) Advances in plant breeding strategies: fruits. Springer, Cham
Rayapuram C, Jensen MK, Maiser F, Shanir JV, Hornshøj H, Rung JH, Gregersen PL, Schweizer P, Collinge DB, Lyngkjær MF (2012) Regulation of basal resistance by a powdery mildew-induced cysteine-rich receptor-like protein kinase in barley. Mol Plant Pathol 13:135–147
Sakamoto T, Deguchi M, Brustolini OJ, Santos AA, Silva FF, Fontes EP (2012) The tomato RLK superfamily: phylogeny and functional predictions about the role of the LRRII-RLK subfamily in antiviral defense. BMC Plant Biol 12:229
Shiu SH, Bleecker AB (2001) Plant receptor-like kinase gene family: diversity, function, and signaling. Sci Signal 2001:e22
Shiu SH, Karlowski WM, Pan R, Tzeng YH, Mayer KFX, Li WH (2004) Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16:1220–1234
Sook LD, Cheon KY, Jae KS, Choong-Min R, Park OK (2017) The arabidopsis cysteine-rich receptor-like kinase crk36 regulates immunity through interaction with the cytoplasmic kinase bik1. Front Plant Sci 8:1856
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 18:763
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
Tan Y, Lv S, Liu X, Gao T, Li T, Wang Y, Wu T, Zhang X, Han Y, Korban SS, Han Z (2017) Development of high-density interspecific genetic maps for the identification of qtls conferring resistance to valsaceratosperma in apple. Euphytica 213:10
Vidhyasekaran P (2015) Plant hormone signaling systems in plant innate immunity. Springer, Dordrecht
Walker JC, Zhang R (1990) Relationship of a putative receptor protein kinase from maize to the S-locus glycoproteins of Brassica. Nature 345:743
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
Wrzaczek M, Brosche M, Salojarvi J, Kangasjarvi S, Idanheimo N, Mersmann S, Robatzek S, Karpinski S, Karpinska B, Kangasjarvi J (2010) Transcriptional regulation of the CRK/DUF26 group of receptor-like protein kinases by ozone and plant hormones inArabidopsis. BMC Plant Biol 10:95–95
Xu X, Yu T, Xu R, Shi Y, Lin X, Xu Q, Qi X, Wen Y, Chen X (2016) Fine mapping of a dominantly inherited powdery mildew resistance major-effect QTL, Pm1.1, in cucumber identifies a 41.1 kb region containing two tandemly arrayed cysteine-rich receptor-like protein kinase genes. Theor Appl Genet 129:507–516
Xu M, Gao X, Chen J, Yin Z, Feng H, Huang L (2017) The feruloyl esterase genes are required for full pathogenicity of the apple tree canker pathogen valsamali. Mol Plant Pathol 19:1353–1363
Yadeta KA, Elmore JM, Creer AY, Feng B, Franco JY, Rufian JS, He P, Coaker G (2017) A cysteine-rich protein kinase associates with a membrane immune complex and the cysteine residues are required for cell death. Plant Physiol 173:771–787
Yang K, Rong W, Qi L, Li J, Wei X, Zhang Z (2013) Isolation and characterization of a novel wheat cysteine-rich receptor-like kinase gene induced by rhizoctonia cerealis. Sci Rep-UK 3:3021
Yeh YH, Chang YH, Huang PY, Huang JB, Zimmerli L (2015) Enhanced arabidopsis pattern-triggered immunity by overexpression of cysteine-rich receptor-like kinases. Front Plant Sci 6:322
Yu X, Du B, Gao Z, Zhang S, Tu X, Chen X, Zhang Z, Qu S (2014) Apple ring rot-responsive putative microRNAs revealed by high-throughput sequencing in Malus. Mol Biol Rep 41:5273–5286
Zhang X, Yang G, Shi R, Han X, Qi L, Wang R, Xiong L, Li G (2013) Arabidopsis cysteine-rich receptor-like kinase 45 functions in the responses to abscisic acid and abiotic stresses. Plant Physiol Biochem 67:189–198
Zhang ZQ, Wang J, Jin W, Ge DD, Liu K, Lü FN, Sun J (2018) Identification and expression analysis of CRK gene family in upland cotton. Sci Agric Sin 51:2442–2461 (in Chinese)
Zhu L, Ni W, Liu S, Cai B, Xing H, Wang S (2017) Transcriptomics analysis of apple leaves in response to Alternaria alternata apple pathotype infection. Front Plant Sci 8:22
Zhu K, Wang X, Liu J, Tang J, Cheng Q, Chen JG, Cheng ZM (2018) The grapevine kinome: annotation, classification and expression patterns in developmental processes and stress responses. Hortic Res-England 5:19
Zuo C, Mao J, Chen Z, Chu M, Duo H, Chen B (2018) RNA sequencing analysis provides new insights into dynamic molecular responses to Valsa mali pathogenicity in apple ‘Changfu No. 2’. Tree Genet Genomes 14:75
Zuo C, Liu Y, Guo Z, Mao J, Chu M, CheN B (2019) Genome-wide annotation and expression responses to biotic stresses of the WALL-ASSOCIATED KINASE-RECEPTOR-LIKE KINASE (WAK-RLK) gene family in Apple (Malus domestica). Eur J Plant Pathol 153:771–785
Funding
This work was supported by the Discipline construction fund project of Gansu Agricultural University (GAU-XKJS-2018-217), the National Natural Science Foundation of China (31860545), and the Science and Technology Major Project of Gansu Province (18ZD2NA006).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing Interests
The authors declare that they have no competing interests.
Consent for Publication
Not applicable.
Ethics Approval and Consent to Participate
Not applicable.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Zuo, C., Liu, H., Lv, Q. et al. Genome-Wide Analysis of the Apple (Malus domestica) Cysteine-Rich Receptor-Like Kinase (CRK) Family: Annotation, Genomic Organization, and Expression Profiles in Response to Fungal Infection. Plant Mol Biol Rep 38, 14–24 (2020). https://doi.org/10.1007/s11105-019-01179-w
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11105-019-01179-w