AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
PDF (11.2 MB)
Collect
Submit Manuscript AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research paper

Genome-wide identification and analysis of cytokinin dehydrogenase/oxidase (CKX) family genes in Brassica oleracea L. reveals their involvement in response to Plasmodiophora brassicae infections

Mingzhao Zhua,bYong WangbShujin LubLimei YangbMu ZhuangbYangyong ZhangbHonghao LvbZhiyuan Fangb( )Xilin Houa( )
State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural University, Nanjing 210095, China
Key Laboratory of Biology and Genetic Improvement of Horticultural Crops, Ministry of Agriculture, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, China

Peer review under responsibility of Chinese Society for Horticultural Science (CSHS) and Institute of Vegetables and Flowers (IVF), Chinese Academy of Agricultural Sciences (CAAS)

Show Author Information

Abstract

Cytokinins are a class of phytohormones that promote cell division and differentiation and are thought to affect plant immunity to multiple pathogens. However, a comprehensive analysis of cytokinin dehydrogenase/oxidase (CKX) family genes in cabbage has not been reported. In this study, a total of 36 CKX genes were identified using a genome-wide search method. Phylogenetic analysis classified these genes into three groups. They were distributed unevenly across nine chromosomes in B. oleracea, and 15 of them did not contain any introns. The results of colinearity analysis showed that 36 CKX gene in Arabidopsis was present in several copies in the Brassica oleracea genome. An analysis of cis-acting elements indicated that all genes possessed at least one stress or hormone responsive cis-acting element. A heatmap of CKX gene expression showed the patterns of expression of these genes in various tissues and organs. Three genes (Bol028363, Bol031036 and Bol018140) were relatively highly expressed in all of the investigated tissues under normal conditions, showing the expression profile of housekeeping genes. Generally, the expression patterns of CKX genes in Jingfeng 1 and Xiangan 336 were quite different under the same treatment. Notably, three genes (Bol020547, Bol028392 and Bol045724) were significantly down-regulated and up-regulated in the susceptible and resistant material, respectively, after inoculation, which may indicate their crucial roles in resistance to clubroot disease. The results provide insights for better understanding the roles of CKX genes in the B. oleraceaP. brassicae interaction.

References

 

Amzallag, G.N., Lerner, H.R., Poljakoff-Mayber, A., 1992. Interaction between mineral nutrients, cytokinin and gibberellic acid during growth of Sorghum at high NaCl salinity. J. Exp. Bot., 43: 81-87.

 

Babosha, A.V., Ryabchenko, A.S., Avetisyan, T.V., 2009. Effect of exogenous cytokinins on dynamics of development and differentiation of infectious structures of the pathogen of wheat powdery mildew. Cell Tissue. Biol., 3: 387-396.

 

Boivin, S., Fonouni-Farde, C., Frugier, F., 2016. How auxin and cytokinin phytohormones modulate root microbe interactions. Front. Plant Sci., 7: 1240.

 

Butcher, D.N., El-Tigani, S., Ingram, D.S., 1974. The role of indole glucosinolates in the club root disease of the Cruciferae. Physiol. Mol. Plant Pathol., 4: 127-140.

 

Davis, J.C., Petrov, D.A., 2004. Preferential duplication of conserved proteins in eukaryotic genomes. PLoS Biol., 2: e55.

 

Dekhuijzen, H.M., 1981. The occurrence of free and bound cytokinins in plasmodia of Plasmodiophora brassicae isolated from tissue cultures of clubroots. Plant Cell Reports, 2: 18-20.

 

Dervinis, C., Frost, C.J., Lawrence, S.D., Novak, N.G., Davis, J.M., 2010. Cytokinin primes plant responses to wounding and reduces insect performance. J. Plant Growth Regul., 29: 289-296.

 

de Vleesschauwer, D., Xu, J., Höfte, M., 2014. Making sense of hormone-mediated defense networking: from rice to Arabidopsis. Front. Plant Sci., 5: 611.

 

Epstein, C.J., 1971. Evolution by gene duplication. Am. J. Hum. Genet., 23: 541.

 

Finn, R.D., Clements, J., Eddy, S.R., 2011. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res., 39: W29-W37.

 

Friedman, R., Hughes, A.L., 2001. Gene duplication and the structure of eukaryotic genomes. Genome Res., 11: 373-381.

 

Galuszka, P., Popelková, H., Werner, T., Frébortová, J., Pospíšilová, H., 2007. Biochemical characterization and histochemical localization of cytokinin oxidases/dehydrogenases from Arabidopsis thaliana expressed in Nicotiana tabaccum L. J. Plant Growth Regul., 26: 255-267.

 

Guo, A., Zhu, Q., Chen, X., Luo, J., 2007. GSDS: a gene structure display server. Hereditas, 29: 1023-1026.

 

Jahn, L., Mucha, S., Bergmann, S., Horn, C., Staswick, P., Steffens, B., Siemens, J., Ludwig-Müller, J., 2013. The clubroot pathogen (Plasmodiophora brassicae) influences auxin signaling to regulate auxin homeostasis in Arabidopsis. Plants, 2: 726-749.

 

Jeffares, D.C., Penkett, C.J., Bähler, J., 2008. Rapidly regulated genes are intron poor. Trends Genet., 24: 375-378.

 

Librado, P., Rozas, J., 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25: 1451-1452.

 

Liu, R.H., Meng, J.L., 2003. MapDraw: a microsoft excel macro for drawing genetic linkage maps based on given genetic linkage data. Hereditas, 25: 317-321.

 

Liu, X., Huang, B., Banowetz, G., 2002. Cytokinin effects on creeping bentgrass responses to heat stress. Crop Sci., 42: 457-465.

 

Liu, X., Zhao, C., Yang, L., Zhang, Y., Wang, Y., Fang, Z., Lv, H., 2020. Genome-wide identification, expression profile of the TIFY gene family in Brassica oleracea var.capitata, and their divergent response to various pathogen infections and phytohormone treatments. Genes, 11: 127.

 

Liu, Z., Lv, Y., Zhang, M., Liu, Y., Kong, L., Zou, M., Lu, G., Cao, J., Yu, X., 2013. Identification expression and comparative genomic analysis of the IPT and CKX gene families in Chinese cabbage (Brassica rapa ssp. pekinensis). BMC Genomics, 14: 594.

 

Lopes-Caitar, V.S., Ccg, D.C.M., Darben, L.M., Kuwahara, M.K., Nepomuceno, A.L., Dias, W.P., Abdelnoor, R.V., Marcelino-Guimarães, F.C., 2013. Genome-wide analysis of the Hsp20 gene family in soybean: comprehensive sequence, genomic organization and expression profile analysis under abiotic and biotic stresses. BMC Genomics, 14: 577.

 

Machanick, P., Bailey, T.L., 2011. MEME-ChIP: motif analysis of large DNA datasets. Bioinformatics, 27: 1696-1697.

 

Maere, S., De Bodt, S., Raes, J., Casneuf, T., Van Montagu, M., Kuiper, M., van de Peer, Y., 2005. Modeling gene and genome duplications in eukaryotes. Proc. Natl. Acad. Sci. USA, 102: 5454-5459.

 

Malinowski, R., Novák, O., Borhan, M.H., Spíchal, L., Strnad, M., Rolfe, S.A., 2016. The role of cytokinins in clubroot disease. Eur. J. Plant Pathol., 145: 543-557.

 

Marchler-Bauer, A., Derbyshire, M.K., Gonzales, N.R., Lu, S., Chitsaz, F., Geer, L.Y., Geer, R.C., He, Jane., Gwadz, M., Hurwitz, D.I., Lanczycki, C.J., Lu, F., Marchler, G.H., Song, J.S., Thanki, N., Wang, Z., Yamashita, R.A., Zhang, D., Zheng, C., Bryant, S.H., 2014. CDD: NCBI's conserved domain database. Nucleic Acids Res., 43: D222-D226.

 

Matsumoto-Kitano, M., Kusumoto, T., Tarkowski, P., Kinoshita-Tsujimura, K., Václavíková, K., Miyawaki, K., Kakimoto, T., 2008. Cytokinins are central regulators of cambial activity. Proc. Natl. Acad. Sci. USA, 105: 20027-20031.

 

Merewitz, E.B., Gianfagna, T., Huang, B.R., 2010. Effects of SAG12-ipt and HSP18.2-ipt expression on cytokinin production, root growth, and leaf senescence in creeping bentgrass exposed to drought stress. J. Am. Soc. Hortic. Sci., 135: 230-239.

 

Mok, D.W.S., Mok, M.C., 2001. Cytokinin metabolism and action. Annu. Rev. Plant Biol., 52: 89-118.

 

Mok, M.C., 1994. Cytokinins and Plant development. Cytokinins: Chemistry, Activity, and Function. CRC Press, Boca Raton: 155–166.

 

Müller, P., Hilgenberg, W., 1986. Isomers of zeatin and zeatin riboside in clubroot tissue: evidence for trans-zeatin bio-synthesis by Plasmodiophora brassicae. Physiol. Plant, 66: 245-250.

 

Nagaharu, U., 1935. Genome analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilization. Jpn. J. Bot., 7: 389-452.

 

Naseem, M., Wölfling, M., Dandekar, T., 2014. Cytokinins for immunity beyond growth, galls and green islands. Trends Plant Sci., 19: 481-484.

 

Ning, Y., Wang, Y., Fang, Z., Zhuang, M., Zhang, Y., Lv, H., Liu, Y., Li, Z., Yang, L., 2018. Identification and characterization of resistance for Plasmodiophora brassicae race 4 in cabbage (Brassica oleracea var. capitata). Austral Plant Pathol., 47: 531-541.

 

Pang, W., Fu, P., Li, X., Zhan, Z., Yu, S., Piao, Z., 2018. Identification and mapping of the Clubroot resistance gene CRd in Chinese cabbage (Brassica rapassp. pekinensis). Front. Plant Sci., 9: 653.

 

Riou-Khamlichi, C., Huntley, R., Jacqmard, A., Murray, J.A.H., 1999. Cytokinin activation of Arabidopsis cell division through a d-type cyclin. Science, 283: 1541-1544.

 

Rivero, R.M., Kojima, M., Gepstein, A., Sakakibara, H., Mittler, R., Gepstein, S., Blumwald, E., 2007. Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proc. Natl. Acad. Sci. USA, 104: 19631-19636.

 

Robin, A.H.K., Hossain, M.R., Kim, H.T., Nou, I.S., Park, J.I., 2019. Role of cytokinins in clubroot disease development. Plant Breed. Biotechnol., 7: 73-82.

 

Rocherieux, J., Glory, P., Giboulot, A., Boury, S., Barbeyron, G., Thomas, G., Manzanares-Dauleux, M.J., 2004. Isolate-specific and broad-spectrum QTLs are involved in the control of clubroot in Brassica oleracea. Theor. Appl. Genet., 108: 1555-1563.

 

Rolfe, S.A., Strelkov, S.E., Links, M.G., Clarke, W.E., Robinson, S.J., Djavaheri, M., Malinowski, R., Haddadi, P., Kagale, S., Parkin, I.A.P., Taheri, A., Borhan, M.H., 2016. The compact genome of the plant pathogen Plasmodiophora brassicae is adapted to intracellular interactions with host Brassica spp. BMC Genomics, 17: 272.

 

Rombauts, S., Dehais, P., Van Montagu, M., Rouze, P., 1999. PlantCARE, a plant cis-acting regulatory element database. Nucleic Acids Res., 27: 295-296.

 

Schmülling, T., Werner, T., Riefler, M., Krupková, E., Manns, I.B.Y., 2003. Structure and function of cytokinin oxidase/dehydrogenase genes of maize, rice, Arabidopsis and other species. J. Plant Res., 116: 241-252.

 

Shang, S., Wu, C., Huang, C., Tie, W., Yan, Y., Ding, Z., Xia, Z., Wang, W., Peng, Ming., Tian, L., Hu, Wei., 2018. Genome-wide analysis of the GRF family reveals their involvement in abiotic stress response in cassava. Genes, 9: 110.

 

Siemens, J., González, M.C., Wolf, S., Hofmann, C., Greiner, S., Du, Y., Rausch, T., Roitsch, T., Ludwig-Müller, J., 2011. Extracellular invertase is involved in the regulation of clubroot disease in Arabidopsis thaliana. Mol. Plant Pathol., 12: 247-262.

 

Siemens, J., Keller, I., Sarx, J., Kunz, S., Schuller, A., Nagel, W., Schmülling, T., Parniske, M., Ludwig-Müller, J., 2006. Transcriptome analysis of Arabidopsis clubroots indicate a key role for cytokinins in disease development. Mol. Plant-Microbe Interact., 19: 480-494.

 

Smigocki, A.C., 1995. Phenotype modification and enhanced tolerance to insect pests by regulated expression of a cytokinin biosynthesis gene. Hortscience, 30: 967-969.

 

Tamura, K., Stecher, G., Peterson, D., Filipski, A., Kumar, S., 2013. Molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol., 30: 2725-2729.

 
Wang, X., Kole, C., 2015. The Brassica rapa Genome. Compendium of Plant Genomes. Springer, Berlin, Heidelberg.
 

Werner, T., Köllmer, I., Bartrina, I., Holst, K., Schmülling, T., 2006. New insights into the biology of cytokinin degradation. Plant Biol., 8: 371.

 

Werner, T., Motyka, V., Laucou, V., Smets, R., van Onckelen, H., Schmülling, T., 2003. Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell, 15: 2532-2550.

 

Williams, P.H., 1966. A system for the determination of races of Plasmodiophora brassicae that infect cabbage and rutabaga. Phytopathology, 56: 624-626.

 

Yao, J.F., An, J.P., You, C.X., Wang, X.F., Hao, Y.J., 2019. Molecular cloning and tolerance identification of apple cytokinin oxidase gene MdCKX7.2. Acta Hortic. Sin., 46: 409-420.

 

Yu, F., Zhang, X., Peng, G., Falk, K.C., Strelkov, S.E., Gossen, B.D., 2017. Genotyping-by-sequencing reveals three QTL for clubroot resistance to six pathotypes of Plasmodiophora brassicae inBrassica rapa. Sci. Rep., 7: 4516.

 

Zhang, H., Zhang, S.J., Li, F., Zhang, S.F., Li, G.L., Ma, X.C., Liu, X.T., Sun, R.F., 2020. Research progress on clubroot disease resistance breeding of Brassica rapa. Acta Hortic. Sin., 47: 1648-1662.

 

Zhang, J., Wu, Y., Feng, H., Ge, W.J., Liu, X.Y., Lü, M.C., Wang, Y.L., Ji, R.Q., 2019. Obtaining and identification of single-spore physiological races of Plasmodiophora brassicae in Williams system. Acta Hortic. Sin., 46: 2415-2422.

 

Zhao, P., Wang, D., Wang, R., Kong, N., Zhang, C., Yang, C., Wu, W., Ma, H., Chen, Q., 2018. Genome-wideanalysis of the potato Hsp20 gene family: identification, genomic organization and expression profiles in response to heat stress. BMC Genomics, 19: 61.

 

Zhou, F., Guo, Y., Qiu, L.J., 2016. Genome-wide identification and evolutionary analysis of leucine-rich repeat receptor-like protein kinase genes in soybean. BMC Plant Biol., 16: 58.

Horticultural Plant Journal
Pages 68-80
Cite this article:
Zhu M, Wang Y, Lu S, et al. Genome-wide identification and analysis of cytokinin dehydrogenase/oxidase (CKX) family genes in Brassica oleracea L. reveals their involvement in response to Plasmodiophora brassicae infections. Horticultural Plant Journal, 2022, 8(1): 68-80. https://doi.org/10.1016/j.hpj.2021.05.003

469

Views

6

Downloads

23

Crossref

20

Web of Science

22

Scopus

1

CSCD

Altmetrics

Received: 24 September 2020
Revised: 23 December 2020
Accepted: 23 April 2021
Published: 24 May 2021
© 2019 Chinese Society for Horticultural Science (CSHS) and Institute of Vegetables and Flowers (IVF), Chinese Academy of Agricultural Sciences (CAAS).

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/)

Return