Abstract
Chickpea (Cicer arietinum L.) is regarded as one of the important grain legumes of the Fabaceae family and being consumed in many countries in the world. Water deficit is the most pivotal environmental factor constraining the worldwide productivity of chickpea. The TCP transcription factors can act as integrators of multiple growth and environmental stimuli. However, no information on this gene family in chickpea with regard to their potential roles in drought responses was reported. In this study, 23 CaTCP genes were identified and characterized in the chickpea genome. First, their major features, including chromosomal distribution, gene duplication, protein features, and conserved domains, were examined. Subsequently, phylogenetic analyses were used to study the relationship of the identified CaTCPs. Next, to gain an insight into the functions of the CaTCP genes, we examined their expression profiles in various tissues at different growth and developmental stages. Furthermore, we carried out expression analyses of the CaTCP genes in chickpea plants subjected to dehydration and abscisic acid (ABA) treatments using real-time quantitative PCR to identify dehydration- and/or ABA-responsive candidate genes that may be promising for further in planta analyses for potential applications in genetic engineering to develop improved drought-tolerant chickpea varieties. We found six and eight CaTCP genes up- and down-regulated, respectively, by at least twofold in chickpea leaves and/or roots by dehydration treatment, among which eight CaTCPs were also responsive to ABA in at least one of the examined organs. CaTCP07 was noted to be the most induced gene upon dehydration and ABA treatments. Our study is the first report on the comprehensive analysis of the CaTCP gene family in chickpea, and provides useful information for further functional characterizations of individual CaTCP genes in chickpea.





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Acharjee S, Sarmah BK (2013) Biotechnologically generating ‘super chickpea’ for food and nutritional security. Plant Sci 207:108–116. https://doi.org/10.1016/j.plantsci.2013.02.003
Agarwal PK, Jha B (2010) Transcription factors in plants and ABA dependent and independent abiotic stress signalling. Biol Plant 54:201–212. https://doi.org/10.1007/s10535-010-0038-7
Aslam M, Mahmood IA, Peoples MB, Schwenke GD, Herridge DF (2003) Contribution of chickpea nitrogen fixation to increased wheat production and soil organic fertility in rain-fed cropping. Biol Fertil Soils 38:59–64. https://doi.org/10.1007/s00374-003-0630-5
Bird LG, Pilkington CL, Saputra A, Serventi L (2017) Products of chickpea processing as texture improvers in gluten-free bread. Food Sci Technol Int 23:690–698. https://doi.org/10.1177/1082013217717802
Bresso EG, Chorostecki U, Rodriguez RE, Palatnik JF, Schommer C (2018) Spatial control of gene expression by miR319-regulated TCP transcription factors in leaf development. Plant Physiol 176:1694–1708. https://doi.org/10.1104/pp.17.00823
Ceylan HA, Türkan I, Sekmen AH (2013) Effect of coronatine on antioxidant enzyme response of chickpea roots to combination of PEG-induced osmotic stress and heat stress. J Plant Growth Regul 32:72–82. https://doi.org/10.1007/s00344-012-9277-5
Chai W, Jiang P, Huang G, Jiang H, Li X (2017) Identification and expression profiling analysis of TCP family genes involved in growth and development in maize. Physiol Mol Biol Plants 23:779–791. https://doi.org/10.1007/s12298-017-0476-1
Chen L, Chen YQ, Ding AM, Chen H, Xia F, Wang WF, Sun YH (2016) Genome-wide analysis of TCP family in tobacco. Genet Mol Res 15:gmr.15027728. https://doi.org/10.4238/gmr.15027728
Cubas P, Lauter N, Doebley J, Coen E (1999) The TCP domain: a motif found in proteins regulating plant growth and development. Plant J 18:215–222. https://doi.org/10.1046/j.1365-313X.1999.00444.x
Danisman S (2016) TCP transcription factors at the interface between environmental challenges and the plant’s growth responses. Front Plant Sci 7:1930. https://doi.org/10.3389/fpls.2016.01930
Deokar AA et al (2015) The CarERF genes in chickpea (Cicer arietinum L.) and the identification of CarERF116 as abiotic stress responsive transcription factor. Funct Integr Genomics 15:27–46. https://doi.org/10.1007/s10142-014-0399-7
Doebley J, Stec A, Hubbard L (1997) The evolution of apical dominance in maize. Nature 386:485–488. https://doi.org/10.1038/386485a0
Dörffling K (2015) The discovery of abscisic acid: a retrospect. J Plant Growth Regul 34:795–808. https://doi.org/10.1007/s00344-015-9525-6
El-Beltagi HS, El-Senousi NA, Ali ZA, Omran AA (2017) The impact of using chickpea flour and dried carp fish powder on pizza quality. PLoS ONE 12:e0183657. https://doi.org/10.1371/journal.pone.0183657
Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2:953–971
Esfahani MN, Sulieman S, Schulze J, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS (2014) Approaches for enhancement of N(2) fixation efficiency of chickpea (Cicer arietinum L.) under limiting nitrogen conditions. Plant Biotechnol J 12:387–397. https://doi.org/10.1111/pbi.12146
Feng ZJ, Xu SC, Liu N, Zhang GW, Hu QZ, Gong YM (2018) Soybean TCP transcription factors: evolution, classification, protein interaction and stress and hormone responsiveness. Plant Physiol Biochem 127:129–142. https://doi.org/10.1016/j.plaphy.2018.03.020
Finn RD et al (2016) The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res 44:D279–D285. https://doi.org/10.1093/nar/gkv1344
Francis A, Dhaka N, Bakshi M, Jung KH, Sharma MK, Sharma R (2016) Comparative phylogenomic analysis provides insights into TCP gene functions in Sorghum. Sci Rep 6:38488. https://doi.org/10.1038/srep38488
Garg R, Sahoo A, Tyagi AK, Jain M (2010) Validation of internal control genes for quantitative gene expression studies in chickpea (Cicer arietinum L.). Biochem Biophys Res Commun 396:283–288. https://doi.org/10.1016/j.bbrc.2010.04.079
Garg R et al (2011) Gene discovery and tissue-specific transcriptome analysis in chickpea with massively parallel pyrosequencing and web resource development. Plant Physiol 156:1661–1678. https://doi.org/10.1104/pp.111.178616
Garg R et al (2016) Transcriptome analyses reveal genotype- and developmental stage-specific molecular responses to drought and salinity stresses in chickpea. Sci Rep 6:19228. https://doi.org/10.1038/srep19228
Gasteiger E, Gattiker A, Hoogland C, Ivanyi I, Appel RD, Bairoch A (2003) ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res 31:3784–3788. https://doi.org/10.1093/nar/gkg563
Gupta RK, Gupta K, Sharma A, Das M, Ansari IA, Dwivedi PD (2017) Health risks and benefits of chickpea (Cicer arietinum) consumption. J Agric Food Chem 65:6–22. https://doi.org/10.1021/acs.jafc.6b02629
Gururani Mayank A, Venkatesh J, Tran LSP (2015) Regulation of photosynthesis during abiotic stress-induced photoinhibition. Mol Plant 8:1304–1320. https://doi.org/10.1016/j.molp.2015.05.005
Ha CV et al (2013) The auxin response factor transcription factor family in soybean: genome-wide identification and expression analyses during development and water stress. DNA Res 20:511–524. https://doi.org/10.1093/dnares/dst027
Ha CV et al (2014) Genome-wide identification and expression analysis of the CaNAC family members in chickpea during development, dehydration and ABA treatments. PLoS ONE 9:e114107. https://doi.org/10.1371/journal.pone.0114107
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297. https://doi.org/10.1093/bioinformatics/btu817
Ilhan E, Buyuk I, Inal B (2018) Transcriptome—scale characterization of salt responsive bean TCP transcription factors. Gene 642:64–73. https://doi.org/10.1016/j.gene.2017.11.021
Jain M, Khurana P, Tyagi AK, Khurana JP (2008) Genome-wide analysis of intronless genes in rice and Arabidopsis. Funct Integr Genomics 8:69–78. https://doi.org/10.1007/s10142-007-0052-9
Jain M et al (2013) A draft genome sequence of the pulse crop chickpea (Cicer arietinum L.). Plant J 74:715–729. https://doi.org/10.1111/tpj.12173
Jukanti AK, Gaur PM, Gowda CL, Chibbar RN (2012) Nutritional quality and health benefits of chickpea (Cicer arietinum L.): a review. Br J Nutr 108:S11–S26. https://doi.org/10.1017/s0007114512000797
Khodadadi M (2013) Effect of drought stress on yield and water relative content in chickpea. Int J Agil Agron Plant Prod 4:1168–1172
Kosugi S, Ohashi Y (1997) PCF1 and PCF2 specifically bind to cis elements in the rice proliferating cell nuclear antigen gene. Plant Cell 9:1607–1619. https://doi.org/10.1105/tpc.9.9.1607
Kosugi S, Ohashi Y (2002) DNA binding and dimerization specificity and potential targets for the TCP protein family. Plant J 30:337–348. https://doi.org/10.1046/j.1365-313X.2002.01294.x
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Le DT, Nishiyama R, Watanabe Y, Mochida K, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS (2011) Genome-wide survey and expression analysis of the plant-specific NAC transcription factor family in soybean during development and dehydration stress. DNA Res 18:263–276. https://doi.org/10.1093/dnares/dsr015
Lei N, Yu X, Li S, Zeng C, Zou L, Liao W, Peng M (2017) Phylogeny and expression pattern analysis of TCP transcription factors in cassava seedlings exposed to cold and/or drought stress. Sci Rep 7:10016. https://doi.org/10.1038/s41598-017-09398-5
Lescot M et al (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. https://doi.org/10.1093/nar/30.1.325
Li W et al (2017) Genome-wide identification and characterization of TCP transcription factor genes in upland cotton (Gossypium hirsutum). Sci Rep 7:10118. https://doi.org/10.1038/s41598-017-10609-2
Lin YF et al (2016) Genome-wide identification and characterization of TCP genes involved in ovule development of Phalaenopsis equestris. J Exp Bot 67:5051–5066. https://doi.org/10.1093/jxb/erw273
Luo D, Carpenter R, Vincent C, Copsey L, Coen E (1996) Origin of floral asymmetry in Antirrhinum. Nature 383:794. https://doi.org/10.1038/383794a0
Ma J, Wang Q, Sun R, Xie F, Jones DC, Zhang B (2014) Genome-wide identification and expression analysis of TCP transcription factors in Gossypium raimondii. Sci Rep 4:6645. https://doi.org/10.1038/srep06645
Ma J, Liu F, Wang Q, Wang K, Jones DC, Zhang B (2016a) Comprehensive analysis of TCP transcription factors and their expression during cotton (Gossypium arboreum) fiber early development. Sci Rep 6:21535. https://doi.org/10.1038/srep21535
Ma X, Ma J, Fan D, Li C, Jiang Y, Luo K (2016b) Genome-wide identification of TCP family transcription factors from Populus euphratica and their involvement in leaf shape regulation. Sci Rep 6:32795. https://doi.org/10.1038/srep32795
Madrigal Y, Alzate JF, Pabon-Mora N (2017) Evolution and expression patterns of TCP genes in Asparagales. Front Plant Sci 8:9. https://doi.org/10.3389/fpls.2017.00009
Manassero NG, Viola IL, Welchen E, Gonzalez DH (2013) TCP transcription factors: architectures of plant form. Biomol Concepts 4:111–127. https://doi.org/10.1515/bmc-2012-0051
Martín-Trillo M, Cubas P (2010) TCP genes: a family snapshot ten years later. Trends Plant Sci 15:31–39. https://doi.org/10.1016/j.tplants.2009.11.003
Mukhopadhyay P, Tyagi AK (2015) OsTCP19 influences developmental and abiotic stress signaling by modulating ABI4-mediated pathways. Sci Rep 5:9998. https://doi.org/10.1038/srep09998
Nicolas M, Cubas P (2016) TCP factors: new kids on the signaling block. Curr Opin Plant Biol 33:33–41. https://doi.org/10.1016/j.pbi.2016.05.006
Osakabe Y, Osakabe K, Shinozaki K, Tran LS (2014) Response of plants to water stress. Front Plant Sci 5:86. https://doi.org/10.3389/fpls.2014.00086
Parapunova V et al (2014) Identification, cloning and characterization of the tomato TCP transcription factor family. BMC Plant Biol 14:157. https://doi.org/10.1186/1471-2229-14-157
Pellicer J, Hidalgo O, Dodsworth S, Leitch IJ (2018) Genome size diversity and its impact on the evolution of land plants. Genes 9:88. https://doi.org/10.3390/genes9020088
Pontes B, Giráldez R, Aguilar-Ruiz JS (2013) Configurable pattern-based evolutionary biclustering of gene expression data. Algorithms Mol Biol 8:4. https://doi.org/10.1186/1748-7188-8-4
Rachwa-Rosiak D, Nebesny E, Budryn G (2013) Chickpeas—composition, nutritional value, health benefits, application to bread and snacks: a review. Crit Rev Food Sci Nutr 55:1137–1145. https://doi.org/10.1080/10408398.2012.687418
Resentini F, Felipo-Benavent A, Colombo L, Blazquez MA, Alabadi D, Masiero S (2015) TCP14 and TCP15 mediate the promotion of seed germination by gibberellins in Arabidopsis thaliana. Mol Plant 8:482–485. https://doi.org/10.1016/j.molp.2014.11.018
Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386. https://doi.org/10.1385/1-59259-192-2:365
Sah SK, Reddy KR, Li J (2016) Abscisic acid and abiotic stress tolerance in crop plants. Front Plant Sci 7:571. https://doi.org/10.3389/fpls.2016.00571
Shi P, Guy KM, Wu W, Fang B, Yang J, Zhang M, Hu Z (2016) Genome-wide identification and expression analysis of the ClTCP transcription factors in Citrullus lanatus. BMC Plant Biol 16:85. https://doi.org/10.1186/s12870-016-0765-9
Singh VK, Garg R, Jain M (2013) A global view of transcriptome dynamics during flower development in chickpea by deep sequencing. Plant Biotechnol J 11:691–701. https://doi.org/10.1111/pbi.12059
Thompson JD, Gibson TJ, Higgins DG (2002) Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinform. https://doi.org/10.1002/0471250953.bi0203s00
Varshney RK et al (2013) Draft genome sequence of chickpea (Cicer arietinum) provides a resource for trait improvement. Nat Biotech 31:240–246. https://doi.org/10.1038/nbt.2491
Verma M, Kumar V, Patel RK, Garg R, Jain M (2015) CTDB: an integrated chickpea transcriptome database for functional and applied genomics. PLoS ONE 10:e0136880. https://doi.org/10.1371/journal.pone.0136880
Vinogradov AE (2001) Mirrored genome size distributions in monocot and dicot plants. Acta Biotheor 49:43–51. https://doi.org/10.1023/a:1010233608680
Wang L et al (2010) Expression profiling and integrative analysis of the CESA/CSL superfamily in rice. BMC Plant Biol 10:282. https://doi.org/10.1186/1471-2229-10-282
Wei W, Hu Y, Cui MY, Han YT, Gao K, Feng JY (2016) Identification and transcript analysis of the TCP transcription factors in the diploid woodland strawberry Fragaria vesca. Front Plant Sci 7:1937. https://doi.org/10.3389/fpls.2016.01937
Xu Z, Shimizu H, Yagasaki Y, Ito S, Zheng Y, Zhou G (2013) Interactive effects of elevated CO2, drought, and warming on plants. J Plant Growth Regul 32:692–707. https://doi.org/10.1007/s00344-013-9337-5
Yao X, Ma H, Wang J, Zhang D (2007) Genome-wide comparative analysis and expression pattern of TCP gene families in Arabidopsis thaliana and Oryza sativa. J Integr Plant Biol 49:885–897. https://doi.org/10.1111/j.1672-9072.2007.00509.x
Zheng Y et al (2016) iTAK: a program for genome-wide prediction and classification of plant transcription factors, transcriptional regulators, and protein kinases. Mol Plant 9:1667–1670. https://doi.org/10.1016/j.molp.2016.09.014
Acknowledgements
Cuong Duy Tran would like to acknowledge the PhD Fellowship funded by the International Program Associate of RIKEN. Our study was partly funded by the Hanoi Pedagogical University 2 under the Grant No. 08/HĐƯT-KHCN to Hong Viet La.
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L-SPT designed the experiment. CDT, HDC, KHN, YW, HVL, and KDT performed the experiments. CDT, HDC, and KHN analyzed the data with the input of L-SPT. HDC and L-SPT wrote the manuscript. All authors read and approved the final manuscript.
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Tran, C.D., Chu, H.D., Nguyen, K.H. et al. Genome-Wide Identification of the TCP Transcription Factor Family in Chickpea (Cicer arietinum L.) and Their Transcriptional Responses to Dehydration and Exogenous Abscisic Acid Treatments. J Plant Growth Regul 37, 1286–1299 (2018). https://doi.org/10.1007/s00344-018-9859-y
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DOI: https://doi.org/10.1007/s00344-018-9859-y

