Research articleGenome-wide characterization of two-component system (TCS) genes in melon (Cucumis melo L.)
Introduction
Cytokinin is a key plant hormone and has been reported to be involved in almost all aspects of plant growth and development, such as seed germination, root and leaf development, flowering, and plant senescence, as well as responses to environmental stimuli (Hwang and Sheen, 2001; Werner and Schmülling, 2009; Fusconi, 2014; Han et al., 2014; Edwards et al., 2018; Kieber and Schaller, 2018). Cytokinin signaling is transduced by a two-component system (TCS) in plants. This system is first reported in bacteria and usually composed of two signaling elements, a histidine kinase (HK) gene family and a response regulator (RR) gene family (Mizuno, 1997; Stock et al., 2000). HK proteins can be phosphorylated and successively transfer the phosphoryl group to a conserved Asp residue in the receiver (Rec) domain of an RR. The phosphorylated RR protein works as a direct or indirect modulator of the activity of downstream genes (Stock et al., 2000; Hwang et al., 2012). Plant TCSs are more complex than most of bacteria TCSs, and a histidine phosphotransfer (HP) gene family has been identified to be responsible for an additional phosphorylation step (Thomason and Kay, 2000; Urao et al., 2000). HP protein functions as a bridge in the transfer of the phosphoryl group between the HK and the RR (Urao et al., 2000; Hwang et al., 2002; Schaller et al., 2008).
TCS signaling has been widely reported in plant kingdoms, such as the model plants Arabidopsis thaliana and rice (Oryza sativa), as well as in some important horticultural crops (Hwang et al., 2002; Pareek et al., 2006; Schaller et al., 2008; Ishida et al., 2009, 2010; Mochida et al., 2010; Chu et al., 2011; Liu et al., 2014; He et al., 2016a, 2016b). The fact that the TCS gene number varies greatly in different plant species indicates that high specialization of TCS members might have occurred over the course of evolution (Liu et al., 2018). Thus, systematic bioinformatics analysis of TCS members should be conducted for more plants, which could benefit our understanding of the evolution and functions of TCS signaling in plants (Koretke et al., 2000; Wuichet et al., 2010; Capra and Laub, 2012).
Melon (Cucumis melo L.) is an important member of the Cucurbitaceae family and has attracted extensive attention from horticultural scientists due to its specific biological properties (Garcia-Mas et al., 2012; Chang et al., 2017). Previous investigations of TCS genes have been performed in cucumber and watermelon, another two members in the Cucurbitaceae family, and a close association has been demonstrated between these TCS genes and some important agricultural traits (He et al., 2016a, 2016b); however, characterization of TCS genes in melon has been largely limited due to the lack of genome data. Recently, the melon genome sequencing project was completed, and its genomic data were released, providing an opportunity to perform genome-wide analysis of TCS genes in melon (Garcia-Mas et al., 2012; Ruggieri et al., 2018).
In our previous study, 44 putative TCS members were identified in melon by analyzing genome data deposited in the Cucurbit Genomics Database (http://cucurbitgenomics.org/organism/3) (Liu et al., 2018). Here, we update the information on the identification and classification of TCS genes by analyzing the improved melon genome data that were deposited in NCBI (https://www.ncbi.nlm.nih.gov/). Based on this updated TCS information, we further analyzed the characteristics of these putative melon TCS genes systematically and explored their responses to exogenous application of cytokinins by quantitative real-time PCR (qRT-PCR). Our comprehensive analysis of melon TCS genes may benefit the functional study of TCS signaling in the future.
Section snippets
Plant materials and hormone treatment
Melon (Cucumis melo L.cv. ‘Yangjiaomi’) plants were grown in the greenhouse of Shandong Agricultural University, Tai'an, Shandong Province, P.R. China from March to July 2017, and regular plant management was performed over the cultivation course. Melon seedlings at 3 weeks after germination were used to examine the expression responses of selected TCS genes to exogenous application of trans-zeatin (tZ). The treatment was performed by spraying 100 μM tZ on the second fully expanded leaves
Identification of TCS proteins in melon
Because of the publication of improved melon genome data (Ruggieri et al., 2018), we first identified putative TCS genes in melon using the same protocol described in our previous study (Liu et al., 2018). In total, 51 putative TCS members were observed in melon; notably, 7 more TCSs were identified in this study than in the previously published study (Liu et al., 2018). These TCS genes were named based on the method used in Chinese cabbage (Liu et al., 2014), cucumber and watermelon (He et
Discussion
Cucurbitaceae crops (melon, cucumber and watermelon) and Physcomitrella patens contain fewer TCS members than other plants (Huang et al., 2009; Ishida et al., 2010; He et al., 2016a; Liu et al., 2018), possibly due to their small genome size and relatively few duplication events during their evolution. It is worth mentioning that no type-C RR was found in melon (Fig. 1C, Table 1). The type-C RR is regarded as the oldest RR and might be the possible evolutionary origin of type-A RRs via
Contribution
L.W. and Z.R. conceived and designed the experiments. Q.S. provided plant material. P.L., S.W., X.W., C.C., Q.L., and C.W. performed the experiments. L.W. and P.L. analyzed the data. L.W., X.Y and R.Z. wrote the manuscript.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
This work was supported by Key R & D plan in Shandong (2018GNC110014), Prospect of Shandong Seed Project, China (2016LZGC033), ‘Taishan Scholar’ Foundation of the People's Government of Shandong Province (ts20130932), China Postdoctoral Science Foundation (2017M612741), National Natural Science Foundation of China (31501781) and Natural Science Foundation of Guangdong Province (2018A030310446).
References (58)
- et al.
Genome-wide single nucleotide polymorphism discovery and the construction of a high-density genetic map for melon (Cucumis melo L.) using genotyping-by-sequencing
Front. Plant Sci.
(2017) - et al.
Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method
Methods
(2001) - et al.
Two-component systems in plant signal transduction
Trends Plant Sci.
(2000) - et al.
Cytokinin action in plant development
Curr. Opin. Plant Biol.
(2009) - et al.
Evolution and phyletic distribution of two-component signal transduction systems
Curr. Opin. Microbiol.
(2010) - et al.
KaKs_Calculator: calculating Ka and Ks through model selection and model averaging
Genom. Proteom. Bioinf.
(2006) - et al.
Evolutionary divergence and convergence in proteins
- et al.
Evolution of two-component signal transduction systems
Annu. Rev. Microbiol.
(2012) - et al.
Genome-wide identification and comparative expression analysis of LEA genes in watermelon and melon genomes
Physiol. Mol. Biol. Plants
(2017) - et al.
Genome-wide identification, classification, and analysis of two-component signal system genes in maize
Genet. Mol. Res.
(2011)
Circadian clock components control daily growth activities by modulating cytokinin levels and cell division‐associated gene expression in Populus trees
Plant Cell Environ.
HMMER web server: interactive sequence similarity searching
Nucleic Acids Res.
Pfam: the protein families database
Nucleic Acids Res.
Identification of a novel cis-element exhibiting cytokinin-dependent protein binding in vitro in the 5’-region of NADPH-protochlorophyllide oxidoreductase gene in cucumber
Plant Mol. Biol.
Regulation of root morphogenesis in arbuscular mycorrhizae: what role do fungal exudates, phosphate, sugars and hormones play in lateral root formation?
Ann. Bot.
A multi-step phosphorelay two-component system impacts on tolerance against dehydration stress in common wheat
Funct. Integr. Genom.
The genome of melon (Cucumis melo L.)
Proc. Natl. Acad. Sci. U.S.A.
Extent of gene duplication in the genomes of drosophila, nematode, and yeast
Mol. Biol. Evol.
Cytokinin pathway mediates APETAKA1 function in the establishment of determinate floral meristems in Arabidopsis
Proc. Natl. Acad. Sci. U.S.A.
Genome-wide identification of two-component system genes in Cucurbitaceae crops and expression profiling analyses in cucumber
Front. Plant Sci.
Genome-wide identification and expression analysis of two-component system genes in tomato
Int. J. Mol. Sci.
Genome-wide analysis of the MADS-box gene family in cucumber
Genome
The genome of the cucumber, Cucumis sativus L
Nat. Genet.
Two-component signal transduction pathways in Arabidopsis
Plant Physiol.
Two-component circuitry in Arabidopsis cytokinin signal transduction
Nature
Cytokinin signaling networks
Annu. Rev. Plant Biol.
A genome-wide compilation of the two-component systems in Lotus japonicus
DNA Res.
Classification of the genes involved in the two-component system of the moss Physcomitrella patens
Biosci. Biotechnol. Biochem.
The effects of repeated whole genome duplication events on the evolution of cytokinin signaling pathway
BMC Evol. Biol.
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These authors contribute equally to this work.