Advertisement

European Journal of Plant Pathology

, Volume 153, Issue 1, pp 153–167 | Cite as

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)

  • Cunwu Zuo
  • Yulian Liu
  • Zhigang Guo
  • Juan Mao
  • Mingyu Chu
  • Baihong ChenEmail author
Article
  • 151 Downloads

Abstract

The WALL ASSOCIATED-KINASE - RECETOR-LIKE KINASE (WAK-RLK) gene family has been reported to act as a sensor for disease. Apple (Malus domestica) can be affected by multiple biotic stresses, such as fungal diseases from Valsa mali (Vm), Alternariaalternata Apple Pathotype (AaAP), and Pythium ultimum (Pu). However, there has been no report of WAK-RLK genes involved in apple biotic stress response. In this paper, we performed a comprehensive study including genome-wide annotation, characterization and gene expression analysis of WAK-RLKs in apple (MdWAK-RLKs). We found 44 members based on structural domain identification. The number of amino acids, molecular weight, and theoretical pI of these identified members ranged from 302 to 998, 33.63 to 110.35 kD, and 5.1 to 9.26, respectively. Members of the family were anchored to 16 out of 17 chromosomes and were classified into six phylogenetic groups. We found two phylogenetic groups specific to the apple genome. Synteny analysis revealed that 11 gene pairs arose from segmental duplications and 7 gene clusters resulted from tandem duplications. Cis-elements in the promoter region of MdWAK-RLKs were found mainly in response to circadian rhythm, hormones, and multiple stresses. The large number of members that showed high expression in multiple tissues and differential expressed in response to stress revealed that the different functional roles of MdWAK-RLKs under physiological or pathological conditions. Several genes, such as MDP0000278283, MDP0000153539, MDP0000170906, and MDP0000251865, were significantly influenced by multiple diseases. This study provides new insights into the potential function of WAK-RLKs in Malus and in Rosaceae and its contribution to disease resistance.

Keywords

The WALL-ASSOCIATED-KINASE - RECETOR-LIKE KINASE (WAK-RLK) Malus domestica bioinformatics analysis disease resistance 

Abbreviations

AaAP

Alternaria alternata Apple Pathotype

RLK

Receptor Like Kinase

WAK-RLKs

The WALL-ASSOCIATED-KINASE - RECETOR-LIKE KINASE

EGF

Epidermal Growth Factor

OGs

Oligogalacturonides

GDR

Genome Database of Rosaceae species

NCBI

The National Center for Biotechnology Information

TAIR

The Arabidopsis Information Resources

MdWAK-RLKs

Malus domestica WAK-RLKs

Pu

Pythium ultimum

qRT-PCR

quantitative Reverse-Transcription-Polymerase Chain Reaction

Vm

Valsa mali

Notes

Funding

This study was funded by the Talent introduction Project of Gansu Agricultural University (GSAU-RCZX201712) and the National Natural Science Foundation of China (31501728) and the Ministry of Agriculture.

Compliance with ethical standards

Conflict of Interest

All authors have received research grants from Gansu Agricultural University. All authors declared that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants performed by any of the authors.

Supplementary material

10658_2018_1591_MOESM1_ESM.docx (17 kb)
ESM 1 (DOCX 16 kb)
10658_2018_1591_MOESM2_ESM.docx (15 kb)
ESM 2 (DOCX 15 kb)

References

  1. 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 Breeding, 129(2), 208–218.CrossRefGoogle Scholar
  2. Baldo, A., Norelli, J. L., Farrell, R. E., Bassett, C. L., Aldwinckle, H. S., & Malnoy, M. (2010). Identification of genes differentially expressed during interaction of resistant and susceptible apple cultivars (Malus × domestica) with Erwinia amylovora. BMC Plant Biology, 10(1), 1–10.CrossRefGoogle Scholar
  3. Bassett, C. L., Baldo, A. M., Moore, J. T., Jenkins, R. M., Soffe, D. S., Wisniewski, M. E., Norelli, J. L., & Jr, R. E. F. (2014). Genes responding to water deficit in apple (malus x domestica borkh.) roots. BMC Plant Biology,14(1), 182.Google Scholar
  4. Benschop, J. J., Mohammed, S., O'Flaherty, M., Heck, A. J., Slijper, M., & Menke, F. L. (2007). Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis. Molecular & Cellular Proteomics, 6(7), 1198–1214.CrossRefGoogle Scholar
  5. Brutus, A., Sicilia, F., Macone, A., Cervone, F., & De Lorenzo, G. (2010). A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proceedings of the National Academy of Sciences of the United States of America, 107(20), 9452–9457.CrossRefGoogle Scholar
  6. Caillaud, M. C., Wirthmueller, L., Sklenar, J., Findlay, K., Piquerez, S. J., Jones, A. M., Robatzek, S., Jones, J. D. G., & Faulkner, C. (2014). The plasmodesmal protein PDLP1 localises to haustoria-associated membranes during downy mildew infection and regulates callose deposition. PLoS Pathogens, 10, e1004496.CrossRefGoogle Scholar
  7. Celton, J. M., Gaillard, S., Bruneau, M., Pelletier, S., Aubourg, S., Martin-Magniette, M. L., Navarro, L., Laurens, F., & Renou, J. P. (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 Phytologist, 203(1), 287–299.CrossRefGoogle Scholar
  8. de Oliveira, L. F. V., Christoff, A. P., de Lima, J. C., de Ross, B. C. F., Sachetto-Martins, G., Margis-Pinheiro, M., & Margis, R. (2014). The Wall-associated Kinase gene family in rice genomes. Plant Science, 229(229), 181–192.Google Scholar
  9. Depuydt, S., & Hardtke, C. S. (2011). Hormone signalling crosstalk in plant growth regulation. Current Biology, 21(9), R365–R373.CrossRefGoogle Scholar
  10. Diener, A. C., & Ausubel, F. M. (2005). Resistance to fusarium oxysproum 1, a dominant Arabidopsis disease-resistance gene, is not race specific. Genetics, 171(1), 305–321.CrossRefGoogle Scholar
  11. Finn, R.D., Bateman, A., Clements, J., Coggill, P., Eberhardt, R.Y., Eddy, S.R., Heger, A., Hetherington, K., Holm, L., Mistry, J., Sonnhammer, E.L.L., Tate, J., & Punta, M. (2014). Pfam: the protein families database. Nucleic acids research, 42(D1), 222–230.Google Scholar
  12. Giorno, F., Guerriero, G., Baric, S., & Mariani, C. (2012). Heat shock transcriptional factors in Malus domestica: identification, classification and expression analysis. BMC Genomics,13, 639Google Scholar
  13. Gendron, J. M., & Wang, Z. Y. (2007). Multiple mechanisms modulate brassinosteroid signaling. Current Opinion in Plant Biology, 10(5), 436–441.CrossRefGoogle Scholar
  14. Hanada, K., Zou, C., Lehti-Shiu, M. D., Shinozaki, K., & Shiu, S. H. (2008). Importance of lineage-specific expansion of plant tandem duplicates in the adaptive response to environmental stimuli. Plant Physiology, 148(2), 993–1003.CrossRefGoogle Scholar
  15. Hou, X., Tong, H., Selby, J., DeWitt, J., Peng, X., & He, Z. H. (2005). Involvement of a cell wall-associated kinase, WAKL4, in Arabidopsis mineral responses. Plant Physiology, 139(4), 1704–1716.CrossRefGoogle Scholar
  16. Hu, B., Jin, J., Guo, A. Y., Zhang, H., Luo, J., Gao, G. 2015. GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics, 31(8), 1296–1297.Google Scholar
  17. Hurni, S., Scheuermann, D., Krattinger, S. G., Kessel, B., Wicker, T., Herren, G., Fitze, M. N., Breen, J., Presterl, T., Ouzunova, M., & Keller, B. (2015). The maize disease resistance gene Htn1 against northern corn leaf blight encodes a wall-associated receptor-like kinase. Proceedings of the National Academy of Sciences of the United States of America, 112(28), 8780–8785.CrossRefGoogle Scholar
  18. Kamber, T., Buchmann, J. P., Pothier, J. F., Smits, T. H., Wicker, T., & Duffy, B. (2016). Fire blight disease reactome: RNA-seq transcriptional profile of apple host plant defense responses to Erwinia amylovora pathogen infection. Scientific Reports, 6.Google Scholar
  19. Kaur, R., Singh, K., & Singh, J. (2013). A root-specific wall-associated kinase gene, HvWAK1, regulates root growth and is highly divergent in barley and other cereals. Functional & Integrative Genomics, 13(2), 167–177.CrossRefGoogle Scholar
  20. Kohorn, B. D. (2001). WAKs; cell wall associated kinases. Current Opinion in Cell Biology, 13(5), 529–533.CrossRefGoogle Scholar
  21. Kohorn, B. D., & Kohorn, S. L. (2012). The cell wall-associated kinases, WAKs, as pectin receptors. Frontiers in Plant Science, 3, 88.CrossRefGoogle Scholar
  22. Kohorn, B. D., Kobayashi, M., Johansen, S., Riese, J., Huang, L. F., Koch, K., Fu, S., Dotson, A., & Byers, N. (2006). An Arabidopsis cell wall-associated kinase required for invertase activity and cell growth. The Plant Journal, 46(2), 307–316.CrossRefGoogle Scholar
  23. Lally, D., Ingmire, P., Tong, H. Y., & He, Z. H. (2001). Antisense expression of a cell wall–associated protein kinase, WAK4, inhibits cell elongation and alters morphology. The Plant Cell, 13(6), 1317–1332.CrossRefGoogle Scholar
  24. 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(21), 2947–2948Google Scholar
  25. Lehti-Shiu, M. D., Zou, C., & Shiu, S. H. (2012). Origin, diversity, expansion history, and functional evolution of the plant Receptor-Like Kinase/Pelle family. In Receptor-Like Kinases in Plants (pp. 1–22). Berlin Heidelberg: Springer.Google Scholar
  26. Leisso, R., Leisso, R., & Mazzola, M. (2016, December). Apple replant disease and the-omics: interaction of apple rootstock metabolome and the soil microbiome. In American Phytopathological Society Annual Meeting (Vol. 106, p. S4).Google Scholar
  27. Lescot, M., Déhais, P., Thijs, G., Marchal, K., Moreau, Y., Peer, Y. V. D., 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 Research, 30(1), 325–327.Google Scholar
  28. Li, H., Zhou, S. Y., Zhao, W. S., Su, S. C., & Peng, Y. L. (2009). A novel wall-associated receptor-like protein kinase gene, OsWAK1, plays important roles in rice blast disease resistance. Plant Molecular Biology, 69(3), 337–346.CrossRefGoogle Scholar
  29. Lim, C. W., Yang, S. H., Shin, K. H., Lee, S. C., & Kim, S. H. (2015). The AtLRK10L1. 2, Arabidopsis ortholog of wheat LRK10, is involved in ABA-mediated signaling and drought resistance. Plant Cell Reports, 34(3), 447–455.CrossRefGoogle Scholar
  30. Mangwanda, R., Myburg, A. A., & Naidoo, S. (2015). Transcriptome and hormone profiling reveals Eucalyptus grandis defence responses against Chrysoporthe austroafricana. BMC Genomics, 16(1), 319.CrossRefGoogle Scholar
  31. Matsubayashi, Y., Ogawa, M., Morita, A., & Sakagami, Y. (2002). An LRR receptor kinase involved in perception of a peptide plant hormone. phytosulfokine. Science, 296(5572), 1470–1472.Google Scholar
  32. Meier, S., Ruzvidzo, O., Morse, M., Donaldson, L., Kwezi, L., & Gehring, C. (2010). The Arabidopsis wall associated kinase-like 10 gene encodes a functional guanylyl cyclase and is co-expressed with pathogen defense related genes. PLOS one, 5(1), e8904.CrossRefGoogle Scholar
  33. Nguyen, Q. N., Lee, Y. S., Cho, L. H., Jeong, H. J., An, G., & Jung, K. H. (2015). Genome-wide identification and analysis of Catharanthus roseus RLK1-like kinases in rice. Planta, 241(3), 603–613.CrossRefGoogle Scholar
  34. Osakabe, Y., Yamaguchi-Shinozaki, K., Shinozaki, K., & Tran, L. S. P. (2013). Sensing the environment: key roles of membrane-localized kinases in plant perception and response to abiotic stress. Journal of Experimental Botany, 64(2), 445–458.CrossRefGoogle Scholar
  35. Peleg, Z., & Blumwald, E. (2011). Hormone balance and abiotic stress tolerance in crop plants. Current Opinion in Plant Biology, 14(3), 290–295.CrossRefGoogle Scholar
  36. Rizzon, C., Ponger, L., & Gaut, B. S. (2006). Striking similarities in the genomic distribution of tandemly arrayed genes in Arabidopsis and rice. PLoS Computational Biology, 2(9), e115.CrossRefGoogle Scholar
  37. Robert-Seilaniantz, A., Grant, M., & Jones, J. D. (2011). Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annual Review of Phytopathology, 49, 317–343.CrossRefGoogle Scholar
  38. Scheer, J. M., & Ryan, C. A. (2002). The systemin receptor SR160 from Lycopersicon peruvianum is a member of the LRR receptor kinase family. Proceedings of the National Academy of Sciences of the United States of America, 99(14), 9585–9590.CrossRefGoogle Scholar
  39. Schultz, J., Milpetz, F., Bork, P., Ponting, C. P. (1998). SMART, a simple modular architecture research tool: identification of signaling domains. Proceedings of the National Academy of Sciences, 95(11), 5857–5864.Google Scholar
  40. Shin, S., Lv, J., Fazio, G., Mazzola, M., & Zhu, Y. (2014). Transcriptional regulation of ethylene and jasmonate mediated defense response in apple (Malus domestica) root during Pythium ultimum infection. Horticulture research, 1, 14053.CrossRefGoogle Scholar
  41. Shin, S., Zheng, P., Fazio, G., Mazzola, M., Main, D., & Zhu, Y. (2016a). Transcriptome changes specifically associated with apple (Malus domestica) root defense response during Pythium ultimum infection. Physiological and Molecular Plant Pathology, 94, 16–26.CrossRefGoogle Scholar
  42. Shin, K. H., Yang, S. H., Lee, J. Y., Lim, C. W., Lee, S. C., Brown, J. W., & Kim, S. H. (2015). Alternative splicing of mini-exons in the arabidopsis leaf rust receptor-like kinase lrk10 genes affects subcellular localisation. Plant Cell Reports, 34(3), 495–505.Google Scholar
  43. Shin, S. Y., Chung, H., Kim, S. Y., & Nam, K. H. (2016b). BRI1-EMS-suppressor 1 gain-of-function mutant shows higher susceptibility to necrotrophic fungal infection. Biochemical and Biophysical Research Communications, 470(4), 864–869.CrossRefGoogle Scholar
  44. Shiu, S. H., Karlowski, W. M., Pan, R., Tzeng, Y. H., Mayer, K. F., & Li, W. H. (2004). Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. The Plant Cell, 16(5), 1220–1234.CrossRefGoogle Scholar
  45. Sivaguru, M., Ezaki, B., He, Z. H., Tong, H., Osawa, H., Baluška, F., Volkmann, D., & Matsumoto, H. (2003). Aluminum-induced gene expression and protein localization of a cell wall-associated receptor kinase in Arabidopsis. Plant Physiology, 132(4), 2256–2266.CrossRefGoogle Scholar
  46. 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. Molecular Biology and Evolution, 28(10), 2731–2739.Google Scholar
  47. Velasco, R., Zharkikh, A., Affourtit, J., Dhingra, A., Cestaro, A., Kalyanaraman, A., Fontana, P., Bhatnagar, S. K., Troggio, M., Pruss, D., Salvi, S., Pindo, M., Baldi, P., Castelletti, S., Cavaiuolo, M., Coppola, G., Costa, F., Cova, V., Ri, A. D., 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, L. M., Gutin, N., Lanchbury, J., Macalma, T., Mitchell, J. T., 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, V. T., King, S. T., Vick, J., Tao, Q., Mraz, A., Stormo, A., Stormo, K., Bogden, R., Ederle, D., Stella, A., Vecchietti, A., Kater, M. M., Masiero, S., Lasserre, P., Lespinasse, Y., Allan, A. C., Bus, V., Chagné, D., Crowhurst, R. N., Gleave, A. P., Lavezzo, E., Fawcett, J. A., Proost, S., Rouzé, P., Sterck, L., Toppo, S., Lazzari, B., Hellens, R. P., Durel, C., Gutin, A., Bumgarner, R. E., Gardiner, S. E., Skolnick, M., Egholm, M., Peer, Y. V., & Salamin, F. (2010). The genome of the domesticated apple (Malus × domestica Borkh.). Nature Genetics, 42(10), 833–839.CrossRefGoogle Scholar
  48. Verica, J. A., & He, Z. H. (2002). The Cell Wall-Associated Kinase (WAK) and WAK-Like Kinase Gene Family. Plant Physiology, 129(2), 455–459.CrossRefGoogle Scholar
  49. Wagner, T. A., & Kohorn, B. D. (2001). Wall-associated kinases are expressed throughout plant development and are required for cell expansion. The Plant Cell, 13(2), 303–318.CrossRefGoogle Scholar
  50. Wang, W., Barnaby, J. Y., Tada, Y., Li, H., Tör, M., Caldelari, D., Lee, D., Fu, X., & Dong, X. (2011). Timing of plant immune responses by a central circadian regulator. Nature, 470(7332), 110–114.CrossRefGoogle Scholar
  51. Wang, Y., Tang, H., DeBarry, J. D., Tan, X., Li, J., Wang, X., Lee, T., 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(7), e49–e49.CrossRefGoogle Scholar
  52. Wang, S., Hu, T., Wang, Y., Luo, Y., Michailides, T. J., & Cao, K. (2016). New understanding on infection processes of Valsa canker of apple in China. European Journal of Plant Pathology, 146(3), 531–540.CrossRefGoogle Scholar
  53. Weigel, D., Ahn, J. H., Blázquez, M. A., Borevitz, J. O., Christensen, S. K., Fankhauser, C., Ferrándiz, C., Kardailsky, I., Malancharuvil, E. J., Neff, M. M., Nguyen, J. T., Sato, S., Wang, Z. Y., Xia, Y., Dixon, R. A., Harrison, M. J., Lamb, C. J., Yanofsky, M. F., & Chory, J. (2000). Activation tagging in Arabidopsis. Plant Physiology, 122(4), 1003–1014.CrossRefGoogle Scholar
  54. Wu, T., Wang, Y., Zheng, Y., Fei, Z., Dandekar, A. M., Xu, K., Han, Z., & Cheng, L. (2015). Suppressing sorbitol synthesis substantially alters the global expression profile of stress response genes in apple (Malus domestica) leaves. Plant and Cell Physiology, 56(9), 1748–1761.CrossRefGoogle Scholar
  55. Yin, Z., Ke, X., Kang, Z., & Huang, L. (2016). Apple resistance responses against Valsa mali revealed by transcriptomics analyses. Physiological and Molecular Plant Pathology, 93, 85–92.  https://doi.org/10.1016/j.pmpp.2016.01.004.CrossRefGoogle Scholar
  56. Zhang, S., Chen, C., Li, L., Meng, L., Singh, J., Jiang, N., Deng, X., He, Z., & Lemaux, P. G. (2005). Evolutionary expansion, gene structure, and expression of the rice wall-associated kinase gene family. Plant Physiology, 139(3), 1107–1124.CrossRefGoogle Scholar
  57. Zhang, K. X., Tian, W. E. N., Jun, D. O. N. G., BAI, T. H., Kun, W. A. N. G., & LI, C. Y. (2016). Comprehensive evaluation of tolerance to alkali stress by 17 genotypes of apple rootstocks. Journal of Integrative Agriculture, 15(7), 1499–1509.CrossRefGoogle Scholar
  58. Zhu, J. K. (2003). Regulation of ion homeostasis under salt stress. Current Opinion in Plant Biology, 6(5), 441–445.CrossRefGoogle Scholar
  59. 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. Frontiers in Plant Science, 8.Google Scholar
  60. Zuo, W., Chao, Q., Zhang, N., Ye, J., Tan, G., Li, B., Xing, Y., Zhang, B., Liu, H., Fengler, K. A., Zhao, J., Zhao, X., Chen, Y., Lai, J., Yan, J., & Xu, M. (2015). A maize wall-associated kinase confers quantitative resistance to head smut. Nature Genetics, 47(2), 151–157.CrossRefGoogle Scholar

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2018

Authors and Affiliations

  • Cunwu Zuo
    • 1
  • Yulian Liu
    • 1
  • Zhigang Guo
    • 1
  • Juan Mao
    • 1
  • Mingyu Chu
    • 1
  • Baihong Chen
    • 1
    Email author
  1. 1.College of HorticultureGansu Agricultural UniversityLanzhouChina

Personalised recommendations