biologia plantarum

International journal on Plant Life established by Bohumil Němec in 1959

Biologia plantarum 63:354-364, 2019 | DOI: 10.32615/bp.2019.041

Differential expressions of citrus CAMTAs during fruit development and responses to abiotic stresses

Z.G. Ouyang, L.F. Mi, H.H. Duan, W. Hu, J.M. Chen, T. Peng, B.L. Zhong*
National Navel Orange Engineering Research Center, College of Life and Environmental Sciences, Gannan Normal University, Ganzhou 341000, P.R. China

Calmodulin-binding transcription activators (CAMTAs) play important roles in plant growth, developmental processes, and responses to abiotic and biotic factors. Recently, five CAMTA members were identified in Citrus sinensis, however, very little is known about the molecular regulation of these CAMTAs in citrus during fruit development and under abiotic stresses. In this study, the different expression profiles of CsCAMTA genes were found in different tissues and different fruit developmental stages. The CsCAMTA genes also displayed distinct expression patterns after heat, cold, salt, and drought stresses. Furthermore, the expressions of CsCAMTA genes were significantly induced by treatments with salicylic acid, methyl jasmonate, or abscisic acid. The green fluorescent protein gene fused with CsCAMTA was specifically expressed in the nucleus of Nicotiana benthamiana cells. Additionally, CsCAMTA proteins can activate or suppress DNA transcription in yeast. These findings provide helpful information for further studies of stress signals in citrus.

Keywords: abscisic acid, Citrus sinensis, cold, drought, heat, jasmonic acid, Nicotiana benthamiana, salicylic acid, salinity, yeast

Accepted: January 9, 2019; Prepublished online: January 9, 2019; Published online: January 19, 2019  Show citation

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Ouyang, Z.G., Mi, L.F., Duan, H.H., Hu, W., Chen, J.M., Peng, T., & Zhong, B.L. (2019). Differential expressions of citrus CAMTAs during fruit development and responses to abiotic stresses. Biologia plantarum, 63, Article 354-364. https://doi.org/10.32615/bp.2019.041
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    References

    1. Aroca, R., Porcel, R., Ruiz-Lozano, J.M.: How does arbuscular mycorrhizal symbiosis regulate root hydraulic properties and plasma membrane aquaporins in Phaseolus vulgaris under drought, cold or salinity stresses? - New Phytol. 173: 808-816, 2007. Go to original source...
    2. Atkinson, N.J., Urwin, P.E.: The interaction of plant biotic and abiotic stresses: from genes to the field. - J. exp. Bot. 63: 3523-3543, 2012. Go to original source...
    3. Bouché, N., Scharlat, A., Snedden, W., Bouchez, D., Fromm, H.: A novel family of calmodulin-binding transcription activators in multicellular organisms. - J. biol. Chem. 277: 21851-21861, 2002. Go to original source...
    4. Cao, X.Q., Jiang, Z.H., Yi, Y.Y., Yi, Y., Ke, L.P., Pei, Z.M., Zhu, S.: Biotic and abiotic stresses activate different Ca2+ permeable channels in Arabidopsis. - Front. Plant Sci. 8: 83, 2017. Go to original source...
    5. Dempsey, D.M.A., Vlot, A.C., Wildermuth, M.C., Klessig, D.F.: Salicylic acid biosynthesis and metabolism. - The Arabidopsis Book 9: e0156, 2011. Go to original source...
    6. Doherty, C.J., Van Buskirk, H.A., Myers, S.J., Thomashow, M.F.: Roles for Arabidopsis CAMTA transcription factors in cold-regulated gene expression and freezing tolerance. - Plant Cell 21: 972-984, 2009. Go to original source...
    7. Du, L., Ali, G.S., Simons, K.A., Hou, J., Yang, T., Reddy, A.S., Poovaiah, B.W.: Ca2+/calmodulin regulates salicylic-acid-mediated plant immunity. - Nature 457: 1154-1158, 2009. Go to original source...
    8. Finkler, A., Ashery-Padan, R., Fromm, H.: CAMTAs: calmodulin-binding transcription activators from plants to human. - FEBS Lett. 581: 3893-3898, 2007. Go to original source...
    9. Fromm, H., Finkler, A.: Repression and de-repression of gene expression in the plant immune response: the complexity of modulation by Ca2+ and calmodulin. - Mol. Plant 8: 671-673, 2015. Go to original source...
    10. Galon, Y., Nave, R., Boyce, J.M., Nachmias, D., Knight, M.R., Fromm, H.: Calmodulin binding transcription activator (CAMTA) 3 mediates biotic defense responses in Arabidopsis. - FEBS Lett. 582: 943-948, 2008. Go to original source...
    11. Gilroy, S., Białasek, M., Suzuki, N., Górecka, M., Devireddy, A.R., Karpiński, S., Mittler, R.: ROS, calcium, and electric signals: key mediators of rapid systemic signaling in plants. - Plant Physiol. 171: 1606-1615, 2016. Go to original source...
    12. Hu, R., Wang, Z., Wu, P., Tang, J., Hou, X.: Identification and abiotic stress analysis of calmodulin-binding transcription activator/signal responsive genes in non-heading Chinese cabbage (Brassica campestris ssp. chinensis Makino). - Plant Omics 8: 141, 2015.
    13. Kim, Y.S., An, C., Park, S., Gilmour, S.J., Wang, L., Renna, L., Brandizzi, F., Grumet, R., Thomashow, M.F.: CAMTA-mediated regulation of salicylic acid immunity pathway genes in Arabidopsis exposed to low temperature and pathogen infection. - Plant Cell 29: 2465-2477, 2017. Go to original source...
    14. Laluk, K., Prasad, K.V.S.K., Savchenko, T., Celesnik, H., Dehesh, K., Levy, M., Mitchell-Olds, T., Reddy, A.S.N.: The calmodulin-binding transcription factor SIGNAL RESPONSIVE1 is a novel regulator of glucosinolate metabolism and herbivory tolerance in Arabidopsis. - Plant Cell Physiol. 53: 2008-2015, 2012. Go to original source...
    15. Lange, A., Mills, R.E., Lange, C.J., Stewart, M., Devine, S.E., Corbett, A.H.: Classical nuclear localization signals: definition, function, and interaction with importin α. - J. biol. Chem. 282: 5101-5105, 2007. Go to original source...
    16. Leng, X., Han, J., Wang, X., Zhao, M., Sun, X., Wang, C., Fang, J.: Characterization of a calmodulin-binding transcription factor from strawberry (Fragaria × ananassa). - Plant Genome 8: 1-12, 2015. Go to original source...
    17. Li, X.H., Huang, L., Zhang, Y.F., Ouyang, Z.G., Hong, Y.B., Zhang, H.J., Li, D.Y., Song, F.M.: Tomato SR/CAMTA transcription factors SlSR1 and SlSR3L negatively regulate disease resistance response and SlSR1L positively modulates drought stress tolerance. - BMC Plant Biol. 14: 286, 2014. Go to original source...
    18. Liu, J.L., Whalley, H.J., Knight, M.R.: Combining modelling and experimental approaches to explain how calcium signatures are decoded by calmodulin-binding transcription activators (CAMTAs) to produce specific gene expression responses. - New Phytol. 208: 174-187, 2015. Go to original source...
    19. Liu, L., White, M.J., MacRae, T.H.: Transcription factors and their genes in higher plants. - Eur. J. Biochem. 262: 247-257, 1999. Go to original source...
    20. Lu, J., Ju, H., Zhou, G., Zhu, C., Erb, M., Wang, X., Wang, P., Lou, Y.: An EAR-motif-containing ERF transcription factor affects herbivore-induced signaling, defense and resistance in rice. - Plant J. 68: 583-596, 2011. Go to original source...
    21. Mitsuda, N., Isono, T., Sato, M.H.: Arabidopsis CAMTA family proteins enhance V-PPase expression in pollen. - Plant Cell Physiol. 44: 975-981, 2003. Go to original source...
    22. Mohanta, T.K., Kumar, P., Bae, H.: Genomics and evolutionary aspect of calcium signaling event in calmodulin and calmodulin-like proteins in plants. - BMC Plant Biol. 17: 38, 2017. Go to original source...
    23. Nie, H., Zhao, C., Wu, G., Wu, Y., Chen, Y., Tang, D.: SR1, a calmodulin-binding transcription factor, modulates plant defense and ethylene-induced senescence by directly regulating NDR1 and EIN3. - Plant Physiol. 158: 1847-1859, 2012. Go to original source...
    24. Pandey, N., Ranjan, A., Pant, P., Tripathi, R.K., Ateek, F., Pandey, H.P., Patre, V.V., Sawant, S.V.: CAMTA 1 regulates drought responses in Arabidopsis thaliana. - BMC Genomics 14: 216, 2013. Go to original source...
    25. Pant, P., Iqbal, Z., Pandey, B.K., Sawant, S.V.: Genome-wide comparative and evolutionary analysis of calmodulin-binding transcription activator (CAMTA) family in Gossypium species. - Sci. Rep. 8: 5573, 2018. Go to original source...
    26. Prasad, K.V.S.K., Abdel-Hameed, A.A.E., Xing, D., Reddy, A.S.N.: Global gene expression analysis using RNA-seq uncovered a new role for SR1/CAMTA3 transcription factor in salt stress. - Sci. Rep. 6: 27021, 2016. Go to original source...
    27. Qiu, Y., Xi, J., Du, L., Suttle, J.C., Poovaiah, B.W.: Coupling calcium/calmodulin-mediated signaling and herbivore-induced plant response through calmodulin-binding transcription factor AtSR1/CAMTA3. - Plant mol. Biol. 79: 89-99, 2012. Go to original source...
    28. Rahman, H., Xu, Y.P., Zhang, X.R., Cai, X.Z.: Brassica napus genome possesses extraordinary high number of CAMTA genes and CAMTA3 contributes to PAMP triggered immunity and resistance to Sclerotinia sclerotiorum. - Front. Plant Sci. 7: 581, 2016a. Go to original source...
    29. Rahman, H., Yang, J., Xu, Y.P., Munyampundu, J.P., Cai, X.Z.: Phylogeny of plant CAMTAs and role of AtCAMTAs in nonhost resistance to Xanthomonas oryzae pv. oryzae. - Front. Plant Sci. 7: 177, 2016b. Go to original source...
    30. Ranty, B., Aldon, D., Cotelle, V., Galaud, J.P., Thuleau, P., Mazars, C.: Calcium sensors as key hubs in plant responses to biotic and abiotic stresses. - Front. Plant Sci. 7: 327, 2016. Go to original source...
    31. Ribaudo, C.M., Curá, J.A., Cantore, M.L.: Activation of a calcium-dependent protein kinase involved in the Azospirillum growth promotion in rice. - World J. Microbiol. Biotechnol. 33: 22, 2017. Go to original source...
    32. Shangguan, L., Wang, X., Leng, X., Liu, D., Ren, G., Tao, R., Zhang, C., Fang, J.: Identification and bioinformatic analysis of signal responsive/calmodulin-binding transcription activators gene models in Vitis vinifera. - Mol. Biol. Rep. 41: 2937-2949, 2014. Go to original source...
    33. Shen, C., Yang, Y., Du, L., Wang, H.Z.: Calmodulin-binding transcription activators and perspectives for applications in biotechnology. - Appl. Microbiol. Biotechnol. 99: 10379-10385, 2015. Go to original source...
    34. Song, K., Backs, J., McAnally, J., Qi, X., Gerard, R.D., Richardson, J.A., Bassel-Duby, R., Olson, E.N.: The transcriptional coactivator CAMTA2 stimulates cardiac growth by opposing class II histone deacetylases. - Cell 125: 453-466, 2006. Go to original source...
    35. Tan, F.C., Swain, S.M.: Functional characterization of AP3, SOC1 and WUS homologues from citrus (Citrus sinensis). - Physiol. Plant. 131: 481-495, 2007. Go to original source...
    36. Tsuda, K., Somssich, I.E.: Transcriptional networks in plant immunity. - New Phytol. 206: 932-947, 2015. Go to original source...
    37. Wahid, A., Close, T.J.: Expression of dehydrins under heat stress and their relationship with water relations of sugarcane leaves. - Biol. Plant. 51: 104-109, 2007. Go to original source...
    38. Wang, G., Zeng, H., Hu, X., Zhu, Y., Chen, Y., Shen, C., Wang, H., Poovaiah, B., Du, L.: Identification and expression analyses of calmodulin-binding transcription activator genes in soybean. - Plant Soil 386: 205-221, 2015. Go to original source...
    39. Wei, M., Xu, X., Li, C.: Identification and expression of CAMTA genes in Populus trichocarpa under biotic and abiotic stress. - Sci. Rep. 7: 7910, 2017. Go to original source...
    40. Xiao, X.H., Yang, M., Sui, J.L., Qi, J.Y., Fang, Y.J., Hu, S.N., Tang, C.R.: The calcium-dependent protein kinase (CDPK) and CDPK-related kinase gene families in Hevea brasiliensis-comparison with five other plant species in structure, evolution, and expression. - FEBS Open Biol. 7: 4-24, 2017. Go to original source...
    41. Xie, X.L., Shen, S.L., Yin, X.R., Xu, Q., Sun, C., Grierson, D., Ferguson, I., Chen, K.S.: Isolation, classification and transcription profiles of the AP2/ERF transcription factor superfamily in citrus. - Mol. Biol. Rep. 41: 4261-4271, 2014. Go to original source...
    42. Yamaguchi-Shinozaki, K., Shinozaki, K.: Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. - Annu. Rev. Plant Biol. 57: 781-803, 2006. Go to original source...
    43. Yang, T., Peng, H., Whitaker, B.D., Conway, W.S.: Characterization of a calcium/calmodulin-regulated SR/CAMTA gene family during tomato fruit development and ripening. - BMC Plant Biol. 12: 19, 2012. Go to original source...
    44. Yang, T., Peng, H., Whitaker, B.D., Jurick, W.M.: Differential expression of calcium/calmodulin-regulated SlSRs in response to abiotic and biotic stresses in tomato fruit. - Physiol. Plant. 148: 445-455, 2013. Go to original source...
    45. Yang, T., Poovaiah, B.W.: A calmodulin-binding/CGCG box DNA-binding protein family involved in multiple signalling pathways in plants. - J. biol. Chem. 277: 45049-45058, 2002. Go to original source...
    46. Yang, Y., Sun, T., Xu, L., Pi, E., Wang, S., Wang, H., Shen, C.: Genome-wide identification of CAMTA gene family members in Medicago truncatula and their expression during root nodule symbiosis and hormone treatments. - Front. Plant Sci. 6: 459, 2015. Go to original source...
    47. Yue, R., Lu, C., Sun, T., Peng, T., Han, X.H., Qi, J.S., Yan, S.F., Tie, S.G.: Identification and expression profiling analysis of calmodulin-binding transcription activator genes in maize (Zea mays L.) under abiotic and biotic stresses. - Front. Plant Sci. 6: 576, 2015. Go to original source...
    48. Zhou, L., Lan, W., Chen, B., Fang, W., Luan, S.: A calcium sensor-regulated protein kinase, CALCINEURIN B-LIKE PROTEIN-INTERACTING PROTEIN KINASE19, is required for pollen tube growth and polarity. - Plant Physiol. 167: 1351-1360, 2015. Go to original source...

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