Genomic characterization and expression profiles of stress-associated proteins (SAPs) in castor bean (Ricinus communis)

doi:10.1016/j.pld.2020.07.010

Abstract

Abstract: Stress-associated proteins (SAPs) are known as response factors to multiple abiotic and biotic stresses in plants. However, the potential physiological and molecular functions of SAPs remain largely unclear. Castor bean (Ricinus communis L.) is one of the most economically valuable non-edible woody oilseed crops, able to be widely cultivated in marginal lands worldwide because of its broad adaptive capacity to soil and climate conditions. Whether SAPs in castor bean plays a key role in adapting diverse soil conditions and stresses remains unknown. In this study, we used the castor bean genome to identify and characterize nine castor bean SAP genes (RcSAP). Structural analysis showed that castor bean SAP gene structures and functional domain types vary greatly, differing in intron number, protein sequence, and functional domain type. Notably, the AN1-C2H2-C2H2 zinc finger domain within RcSAP9 has not been often observed in other plant families. High throughput RNA-seq data showed that castor bean SAP gene profiles varied among different tissues. In addition, castor bean SAP gene expression varied in response to different stresses, including salt, drought, heat, cold and ABA and MeJA, suggesting that the transcriptional regulation of castor bean SAP genes might operate independently of each other, and at least partially independent from ABA and MeJA signal pathways. Cis-element analyses for each castor bean SAP gene showed that no common cis-elements are shared across the nine castor bean SAP genes. Castor bean SAPs were localized to different regions of cells, including the cytoplasm, nucleus, and cytomembrane. This study provides a comprehensive profile of castor bean SAP genes that advances our understanding of their potential physiological and molecular functions in regulating growth and development and their responses to different abiotic stresses.

Key words: Castor bean, Genomic characterization, Stress-associated proteins, Expression profile

Zaiqing Wang, Jingge Kuang, Bing Han, Suiyun Chen, Aizhong Liu. Genomic characterization and expression profiles of stress-associated proteins (SAPs) in castor bean (Ricinus communis)[J]. Plant Diversity, 2021, 43(02): 152-162.

References

Ben, S.R., Fabre, D., Mieulet, D., et al., 2012. Expression of the Aeluropus littoralis AlSAP gene in rice confers broad tolerance to abiotic stresses through maintenance of photosynthesis. Plant Cell Environ. 35, 626-643.
Ben, S.R., Farhat, K.A., Ben, H.N., et al., 2018. The LmSAP gene isolated from the halotolerant Lobularia maritima improves salt and ionic tolerance in transgenic tobacco lines. Funct. Plant Biol. 45, 378-390.
Brown, A.P., Kroon, J.T., Swarbreck, D., et al., 2012. Tissue-specific whole transcriptome sequencing in castor, directed at understanding triacylglycerol lipid biosynthetic pathways. PLoS One 7, e30100.
Chatre, L., Brandizzi, F., Hocquellet, A., et al., 2005. Sec22 and Memb11 are v-SNAREs of the anterograde endoplasmic reticulum-Golgi pathway in tobacco leaf epidermal cells. Plant Physiol. 139, 1244-1254.
Dansana, P.K., Kothari, K.S., Vij, S., et al., 2014. OsiSAP1 overexpression improves water-deficit stress tolerance in transgenic rice by affecting expression of endogenous stress-related genes. Plant Cell Rep. 33, 1425-1440.
Dixit, A., Tomar, P., Vaine, E., et al., 2018. A stress-associated protein, AtSAP13, from Arabidopsis thaliana provides tolerance to multiple abiotic stresses. Plant Cell Environ. 41, 1171-1185.
Dixit, A.R., Dhankher, O.P., 2011. A novel stress-associated protein ‘AtSAP10’ from Arabidopsis thaliana confers tolerance to nickel, manganese, zinc, and high temperature stress. PLoS One 6, e20921.
Gao, W., Long, L., Tian, X., et al., 2016. Genome-wide identification and expression analysis of stress-associated proteins (SAPs) containing A20/AN1 zinc finger in cotton. Mol. Genet. Genom. 291, 2199-2213.
Giri, J., Dansana, P.K., Kothari, K.S., et al., 2013. SAPs as novel regulators of abiotic stress response in plants. Bioessays 35, 639-648.
Giri, J., Vij, S., Dansana, P.K., et al., 2011. Rice A20/AN1 zinc-finger containing stressassociated proteins (SAP1/11) and a receptor-like cytoplasmic kinase(OsRLCK253) interact via A20 zinc-finger and confer abiotic stress tolerance in transgenic Arabidopsis plants. New Phytol. 191, 721-732.
Hu, B., Jin, J., Guo, A.Y., et al., 2015. GSDS 2.0:an upgraded gene feature visualization server. Bioinformatics 31, 1296-1297.
Huang, J., Wang, M.M., Jiang, Y., et al., 2008. Expression analysis of rice A20/AN1-type zinc finger genes and characterization of ZFP177 that contributes to temperature stress tolerance. Gene 420, 135-144.
Jia, H., Li, J., Zhang, J., et al., 2016. Genome-wide survey and expression analysis of the stress-associated protein gene family in desert poplar, Populus euphratica.Tree Genet. Genomes 12, 1-16.
Kang, M., Abdelmageed, H., Lee, S., et al., 2013. AtMBP-1, an alternative translation product of LOS2, affects abscisic acid responses and is modulated by the E3 ubiquitin ligase AtSAP5. Plant J. 76, 481-493.
Kang, M., Fokar, M., Abdelmageed, H., et al., 2011. Arabidopsis SAP5 functions as a positive regulator of stress responses and exhibits E3 ubiquitin ligase activity.Plant Mol. Biol. 75, 451-466.
Kang, M., Lee, S., Abdelmageed, H., et al., 2017. Arabidopsis stress associated protein 9 mediates biotic and abiotic stress responsive ABA signaling via the proteasome pathway. Plant Cell Environ. 40, 702-716.
Kanneganti, V., Gupta, A.K., 2008. Overexpression of OsiSAP8, a member of stress associated protein (SAP) gene family of rice confers tolerance to salt, drought and cold stress in transgenic tobacco and rice. Plant Mol. Biol. 66, 445-462.
Kim, G.D., Cho, Y.H., Yoo, S.D., 2015. Regulatory functions of evolutionarily conserved AN1/A20-like Zinc finger family proteins in Arabidopsis stress responses under high temperature. Biochem. Biophys. Res. Commun. 457, 213-220.
Kumar, S., Stecher, G., Tamura, K., 2016. MEGA7:molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870-1874.
Lai, W., Zhou, Y., Pan, R., et al., 2020. Identification and expression analysis of stressassociated proteins (SAPs) containing A20/AN1 zinc finger in cucumber. Plants 9, 400-415.
Mukhopadhyay, A., Vij, S., Tyagi, A.K., 2004. Overexpression of a zinc-finger protein gene from rice confers tolerance to cold, dehydration, and salt stress in transgenic tobacco. Proc. Natl. Acad. Sci. USA 101, 6309-6314.
Qiu, L., Yang, C., Tian, B., et al., 2010. Exploiting EST databases for the development and characterization of EST-SSR markers in castor bean (Ricinus communis L.).BMC Plant Biol. 10, 278.
Sharma, G., Giri, J., Tyagi, A.K., 2015. Rice OsiSAP7 negatively regulates ABA stress signalling and imparts sensitivity to water-deficit stress in Arabidopsis. Plant Sci. 237, 80-92.
Solanke, A.U., Sharma, M.K., Tyagi, A.K., et al., 2009. Characterization and phylogenetic analysis of environmental stress-responsive SAP gene family encoding A20/AN1 zinc finger proteins in tomato. Mol. Genet. Genom. 282, 153-164.
Sreedharan, S., Shekhawat, U.K., Ganapathi, T.R., 2012. MusaSAP1, a A20/AN1 zinc finger gene from banana functions as a positive regulator in different stress responses. Plant Mol. Biol. 80, 503-517.
Ströher, E., Wang, X.J., Roloff, N., et al., 2009. Redox-dependent regulation of the stress-induced zinc-finger protein SAP12 in Arabidopsis thaliana. Mol. Plant 2, 357-367.
Tang, C., Yang, M., Fang, Y., et al., 2016. The rubber tree genome reveals new insights into rubber production and species adaptation. Native Plants 2, 16073-16082.
Tyagi, H., Jha, S., Sharma, M., et al., 2014. Rice SAPs are responsive to multiple biotic stresses and overexpression of OsSAP1, an A20/AN1 zinc-finger protein, enhances the basal resistance against pathogen infection in tobacco. Plant Sci. 225, 68-76.
Vij, S., Tyagi, A.K., 2006. Genome-wide analysis of the stress associated protein(SAP) gene family containing A20/AN1 zinc-finger(s) in rice and their phylogenetic relationship with Arabidopsis. Mol. Genet. Genom. 276, 565-575.
Wang, C., Li, G.R., Zhang, Z.Y., et al., 2013a. Genetic diversity of castor bean (Ricinus communis L.) in Northeast China revealed by ISSR markers. Biochem. Systemat.Ecol. 51, 301-307.
Wang, Y., Zhang, L., Zhang, L., et al., 2013b. A novel stress-associated protein SbSAP14 from Sorghum bicolor confers tolerance to salt stress in transgenic rice.Mol. Breed. 32, 437-449.
Wang, Z., Yang, C., Chen, H., et al., 2018. Multi-gene co-expression can improve comprehensive resistance to multiple abiotic stresses in Brassica napus L. Plant Sci. 274, 410-419.
Xu, W., Chen, Z., Ahmed, N., et al., 2016. Genome-wide identification, evolutionary analysis, and stress responses of the GRAS gene family in castor beans. Int. J.Mol. Sci. 17, 1004.
Xu, W., Li, F., Ling, L., et al., 2013. Genome-wide survey and expression profiles of the AP2/ERF family in castor bean (Ricinus communis L.). BMC Genom. 14, 785.
Yin, M., Wang, Y., Zhang, L., et al., 2017. The Arabidopsis Cys2/His2 zinc finger transcription factor ZAT18 is a positive regulator of plant tolerance to drought stress. J. Exp. Bot. 68, 2991-3005.
Yu, A., Li, F., Xu, W., et al., 2019. Application of a high-resolution genetic map for chromosome-scale genome assembly and fine QTLs mapping of seed size and weight traits in castor bean. Sci. Rep. 9, 11950-11960.
Yu, J., Ke, T., Tehrim, S., et al., 2015. PTGBase:an integrated database to study tandem duplicated genes in plants. Database 15, 1-10.
Zhang, X., Zheng, W., Cao, X., et al., 2019. Genomic analysis of stress associated proteins in soybean and the role of GmSAP16 in abiotic stress responses in Arabidopsis and Soybean. Front. Plant Sci. 10, 1453-1471.
Zhang, Y., Lan, H., Shao, Q., et al., 2016. An A20/AN1-type zinc finger protein modulates gibberellins and abscisic acid contents and increases sensitivity to abiotic stress in rice (Oryza sativa). J. Exp. Bot. 67, 315-326.
Zhou, Y., Zeng, L., Chen, R., et al., 2018. Genome-wide identification and characterization of stress-associated protein (SAP) gene family encoding A20/AN1 zinc-finger proteins in Medicago truncatula. Arch. Biol. Sci. 70, 87-98.
Zouari, N., Ben Saad, R., Legavre, T., et al., 2007. Identification and sequencing of ESTs from the halophyte grass Aeluropus littoralis. Gene 404, 61-69.

[1]	Qing Tan, Bing Han, Mohammad Enamul Haque, Ye-Lan Li, Yue Wang, Di Wu, Shi-Bo Wu, Ai-Zhong Liu. The molecular mechanism of WRINKLED1 transcription factor regulating oil accumulation in developing seeds of castor bean [J]. Plant Diversity, 2023, 45(04): 469-478.
[2]	Wen-Bo Wang, Tao Ao, Yan-Yu Zhang, Di Wu, Wei Xu, Bing Han, Ai-Zhong Liu. Genome-wide analysis of the B3 transcription factors reveals that RcABI3/VP1 subfamily plays important roles in seed development and oil storage in castor bean (Ricinus communis) [J]. Plant Diversity, 2022, 44(02): 201-212.
[3]	Qin Yu, Simin Hu, Jiancan Du, Yongping Yang, Xudong Sun. Genome-wide identification and characterization of the lateral organ boundaries domain gene family in Brassica rapa var. rapa [J]. Plant Diversity, 2020, 42(01): 52-60.
[4]	AO Tao-, LIAO Xiao-Jia-, XU Wei-, LIU Ai-Zhong. Identification and Characterization of GATA Gene Family in Castor Bean (Ricinus communis) [J]. Plant Diversity, 2015, 37(4): 453-462.
[5]	HAN Xiao-, WANG Hou-Ping-, BO Jin-Jing-, HU Yan-Ru-, CHEN Xiao-Lan-**, YU Di-Qiu. Arabidopsis WRKY8 Transcription FactorAssociated Genes VQ10 and VQ11 are Responsive to Multiple Abiotic Stresses [J]. Plant Diversity, 2015, 37(06): 760-766.