Genome-wide investigation of Hydroxycinnamoyl CoA: Shikimate Hydroxycinnamoyl Transferase (HCT) gene family in Carthamus tinctorius L.

Sun FAN; Naveed AHMAD; Jin  LIBO; Zhang XINYUE; Ma XINTONG; Nguyen Q. V. HOANG; Ali I. MALLANO; Wang NAN; Yang  ZHUODA; Liu XIUMING; Yao NA

doi:10.15835/nbha49312489

Authors

Sun FAN Jilin Agricultural University, Ministry of Education Engineering Research Center of Bioreactor and Pharmaceutical Development, Changchun 130118 (CN)
Naveed AHMAD Jilin Agricultural University, Ministry of Education Engineering Research Center of Bioreactor and Pharmaceutical Development, Changchun 130118; Shandong Academy of Agricultural Sciences, Biotechnology Research Center, Shandong Provincial Key, Laboratory of Crop Genetic Improvement, Ecology and Physiology, Jinan 250100 (CN)
Jin LIBO Wenzhou University, Institute of Life Sciences, Wenzhou 325035;Wenzhou University, Biomedical Collaborative Innovation Center of Zhejiang Province, Wenzhou, Zhejiang 325035 (CN)
Zhang XINYUE Jilin Agricultural University, Ministry of Education Engineering Research Center of Bioreactor and Pharmaceutical Development, Changchun 130118 (CN)
Ma XINTONG Jilin Agricultural University, Ministry of Education Engineering Research Center of Bioreactor and Pharmaceutical Development, Changchun 130118 (CN)
Nguyen Q. V. HOANG Jilin Agricultural University, Ministry of Education Engineering Research Center of Bioreactor and Pharmaceutical Development, Changchun 130118 (CN)
Ali I. MALLANO Shandong Academy of Agricultural Sciences, Biotechnology Research Center, Shandong Provincial Key, Laboratory of Crop Genetic Improvement, Ecology and Physiology, Jinan 250100 (CN)
Wang NAN Jilin Agricultural University, Ministry of Education Engineering Research Center of Bioreactor and Pharmaceutical Development, Changchun 130118 (CN)
Yang ZHUODA Jilin Agricultural University, Ministry of Education Engineering Research Center of Bioreactor and Pharmaceutical Development, Changchun 130118 (CN)
Liu XIUMING Jilin Agricultural University, Ministry of Education Engineering Research Center of Bioreactor and Pharmaceutical Development, Changchun 130118, (CN)
Yao NA Jilin Agricultural University, Ministry of Education Engineering Research Center of Bioreactor and Pharmaceutical Development, Changchun 130118 (CN)

DOI:

https://doi.org/10.15835/nbha49312489

Keywords:

abiotic stress, Carthamus tinctorius, expression diversity, HCT gene family, monolignol biosynthesis

Abstract

Hydroxycinnamoyl-CoA: shikimate hydroxycinnamoyl transferase (HCT) is mainly associated with monolignol biosynthesis, a central precursor to producing guaiacyl and syringyl lignins in plants. However, the explicit regulatory mechanism of HCT-mediated monolignol biosynthesis in plants still remained unclear. Here, the genome-wide analysis of the HCT gene family in Carthamus tinctorius as a target for understanding growth, development, and stress-responsive mechanisms was investigated. A total of 82 CtHCT genes were identified and characterized. Most of the CtHCTs proteins demonstrated the presence of two common conserved domains, including HXXXD and DFGWG. In addition, the conserved structure of protein motifs, PPI network, cis-regulatory units, and gene structure analysis demonstrated several genetic determinants reflecting the wide range of functional diversity of CtHCT-encoding genes. The observed expression analysis of CtHCT genes in different flowering stages under normal conditions partially highlighted their putative roles in plant growth and development pathways. Moreover, CtHCT genes appeared to be associated with abiotic stress responses as validated by the expression profiling in various flowering phases under light irradiation and MeJA treatment. Altogether, these findings provide new insights into identifying crucial molecular targets associated with plant growth and development and present practical information for understanding abiotic stress-responsive mechanisms in plants.

References

Bhardwaj R, Handa N, Sharma R, Kaur H, Kohli S, Kumar V, Kaur P (2014). Lignins and abiotic stress: an overview. Physiological Mechanisms and Adaptation Strategies in Plants Under Changing Environment. Springer, pp 267-296. https://doi.org/10.1007/978-1-4614-8591-9_10

Chao N, Qi Q, Li S, Ruan B, Jiang X, Gai Y (2021). Characterization and functional analysis of the Hydroxycinnamoyl-CoA: shikimate hydroxycinnamoyl transferase (HCT) gene family in poplar. PeerJ 9:e10741.

Chiang YC, Levsh O, Lam CK, Weng JK, Wang Y (2018). Structural and dynamic basis of substrate permissiveness in hydroxycinnamoyltransferase (HCT). PLoS Computational Biology 14(10):e1006511. https://doi.org/10.1371/journal.pcbi.1006511

Chowdhury EM, Choi BS, Park SU, Lim HS, Bae H (2012). Transcriptional analysis of hydroxycinnamoyl transferase (HCT) in various tissues of Hibiscus cannabinus in response to abiotic stress conditions. Plant Omics 5(3):305.

Conesa A, Götz S (2008). Blast2GO: A comprehensive suite for functional analysis in plant genomics. International Journal of Plant Genomics 2008:619832. https://doi.org/10.1155/2008/619832

D’Auria JC (2006). Acyltransferases in plants: a good time to be BAHD. Current Opinion in Plant Biology 9(3):331-340. https://doi.org/10.1016/j.pbi.2006.03.016

Dang HQ, Tran NQ, Tuteja R, Tuteja N (2011). Promoter of a salinity and cold stress-induced MCM6 DNA helicase from pea. Plant Signaling and Behavior 6(7):1006-1008. https://doi.org/10.4161/psb.6.7.15502

Escamilla-Treviño LL, Shen H, Hernandez T, Yin Y, Xu Y, Dixon RA (2014). Early lignin pathway enzymes and routes to chlorogenic acid in switchgrass (Panicum virgatum L.). Plant Molecular Biology 84(4-5):565-576. https://doi.org/10.1007/s11103-013-0152-y

Eudes A, Pereira JH, Yogiswara S, Wang G, Teixeira Benites V, Baidoo EE, … Loqué D (2016). Exploiting the substrate promiscuity of hydroxycinnamoyl-CoA: shikimate hydroxycinnamoyl transferase to reduce lignin. Plant and Cell Physiology 57(3):568-579. https://doi.org/10.1093/pcp/pcw016

Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, … Sangrador-Vegas A (2015). The Pfam protein families database: towards a more sustainable future. Nucleic Acids Research 44(D1):D279-D285. https://doi.org/10.1093/nar/gkv1344

Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2014). GSDS 2.0: an upgraded gene features visualization server. Bioinformatics 31(8):1296-1297. https://doi.org/10.1093/bioinformatics/btu817

Initiative AG (2000). Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408(6814):796. https://doi.org/10.1038/35048692

Lepelley M, Cheminade G, Tremillon N, Simkin A, Caillet V, McCarthy J (2007). Chlorogenic acid synthesis in coffee: An analysis of CGA content and real-time RT-PCR expression of HCT, HQT, C3H1, and CCoAOMT1 genes during grain development in C. canephora. Plant Science 172(5):978-996. https://doi.org/10.1016/j.plantsci.2007.02.004

Livak KJ, Schmittgen TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25(4):402-408. https://doi.org/10.1006/meth.2001.1262

Ma C, Zhang H, Li J, Tao S, Qiao X, Korban SS, Zhang S, Wu J (2017). Genome-wide analysis and characterization of molecular evolution of the HCT gene family in pear (Pyrus bretschneideri). Plant Systematics and Evolution 303(1):71-90. https://doi.org/10.1007/s00606-016-1353-z

Payyavula RS, Shakya R, Sengoda VG, Munyaneza JE, Swamy P, Navarre DA (2015). Synthesis and regulation of chlorogenic acid in potato: Rerouting phenylpropanoid flux in HQT‐silenced lines. Plant Biotechnology Journal 13(4):551-564. https://doi.org/10.1111/pbi.12280

Roh JS, Han JY, Kim, JH, Hwang JK (2004). Inhibitory effects of active compounds isolated from safflower (Carthamus tinctorius L.) seeds for melanogenesis. Biological and Pharmaceutical Bulletin 27(12):1976-1978. https://doi.org/10.1248/bpb.27.1976

Shadle G, Chen F, Reddy MS, Jackson L, Nakashima J, Dixon RA (2007). Down-regulation of hydroxycinnamoyl CoA: shikimate hydroxycinnamoyl transferase in transgenic alfalfa affects lignification, development and forage quality. Phytochemistry 68(11):1521-1529.

Shi R, Sun YH, Li Q, Heber S, Sederoff R, Chiang VL (2009). Towards a systems approach for lignin biosynthesis in Populus trichocarpa: transcript abundance and specificity of the monolignol biosynthetic genes. Plant and Cell Physiology 51(1):144-163. https://doi.org/10.1093/pcp/pcp175

Shinya T, Hayashi K, Onogi S, Kawaoka A (2014). Transcript level analysis of lignin and flavonoid biosynthesis related genes in Eucalyptus globulus. American Journal of Plant Sciences 5(18):2764. https://doi.org/10.4236/ajps.2014.518293

Shulaev V, Sargent DJ, Crowhurst RN, Mockler TC, Folkerts O, Delcher AL, … Mane SP (2011). The genome of woodland strawberry (Fragaria vesca). Nature Genetics 43(2):109. https://doi.org/10.1038/ng.740

Sonnante G, D’Amore R, Blanco E, Pierri CL, De Palma M, Luo J, … Martin C (2010). Novel hydroxycinnamoyl-coenzyme A quinate transferase genes from artichoke are involved in the synthesis of chlorogenic acid. Plant Physiology 153(3):1224-1238. https://doi.org/10.1104/pp.109.150144

Sullivan M (2009). A novel red clover hydroxycinnamoyl transferase has enzymatic activities consistent with a role in phaselic acid biosynthesis. Plant Physiology 150(4):1866-1879. https://doi.org/10.1104/pp.109.136689

Sun CH, Yang CY, Tzen JT (2018). Molecular identification and characterization of hydroxycinnamoyl transferase in tea plants (Camellia sinensis L.). International Journal of Molecular Sciences 19(12):3938. https://doi.org/10.3390/ijms19123938

Tamagnone L, Merida A, Parr A, Mackay S, Culianez-Macia FA, Roberts K, Martin C (1998). The AmMYB308 and AmMYB330 transcription factors from Antirrhinum regulate phenylpropanoid and lignin biosynthesis in transgenic tobacco. The Plant Cell 10(2):135-154. https://doi.org/10.1105/tpc.10.2.135

Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28(10):2731-2739. https://doi.org/10.1093/molbev/msr121

Tohge T, Watanabe M, Hoefgen R, Fernie AR (2013). The evolution of phenylpropanoid metabolism in the green lineage. Critical Reviews In Biochemistry and Molecular Biology 48(2):123-152. https://doi.org/10.3109/10409238.2012.758083

Torabi B, Soltani E, Archontoulis SV, Rabii A (2016). Temperature and water potential effects on Carthamus tinctorius L. seed germination: measurements and modeling using hydrothermal and multiplicative approaches. Brazilian Journal of Botany 39(2):427-436. https://doi.org/10.1007/s40415-015-0243-x

Tripathi R, Agrawal S (2013). Evaluation of changes in lipid peroxidation, ROS production, surface structures, secondary metabolites and yield of linseed (Linum usitatissimum L.) under individual and combined stress of ultraviolet-B and ozone using open top chambers. Indian Journal of Biochemistry and Biophysics 50(4):318-325.

Tsai CJ, Harding SA, Tschaplinski TJ, Lindroth RL, Yuan Y (2006). Genome‐wide analysis of the structural genes regulating defense phenylpropanoid metabolism in Populus. New Phytologist 172(1):47-62. https://doi.org/10.1111/j.1469-8137.2006.01798.x

Vanholme B, Cesarino I, Goeminne G, Kim H, Marroni F, Van Acker R, … Pinosio S (2013). Breeding with rare defective alleles (BRDA): a natural Populus nigra HCT mutant with modified lignin as a case study. New Phytologist 198(3):765-776. https://doi.org/10.1111/nph.12179

Vanholme R, De Meester B, Ralph J, Boerjan W (2019). Lignin biosynthesis and its integration into metabolism. Current Opinion in Biotechnology 56:230-239. https://doi.org/10.1016/j.copbio.2019.02.018

Varbanova M, Porter K, Lu F, Ralph J, Hammerschmidt R, Jones AD, Day B (2011). Molecular and biochemical basis for stress-induced accumulation of free and bound p-coumaraldehyde in cucumber. Plant Physiology 157(3):1056-1066. https://doi.org/10.1104/pp.111.184358

Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, … Pruss D (2010). The genome of the domesticated apple (Malus × domestica Borkh.). Nature Genetics 42(10):833. https://doi.org/10.1038/ng.654

Verde I, Abbott AG, Scalabrin S, Jung S, Shu S, Marroni F, … Cattonaro F (2013). The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nature Genetics 45(5):487. https://doi.org/10.1038/ng.2586

Wagner A, Ralph J, Akiyama T, Flint H, Phillips L, Torr K, Nanayakkara B, Te Kiri L (2007). Exploring lignification in conifers by silencing hydroxycinnamoyl-CoA: shikimate hydroxycinnamoyltransferase in Pinus radiata. Proceedings of the National Academy of Sciences 104(28):11856-11861. https://doi.org/10.1073/pnas.0701428104

Wang GF, He Y, Strauch R, Olukolu BA, Nielsen D, Li X, Balint-Kurti PJ (2015). Maize homologs of hydroxycinnamoyltransferase, a key enzyme in lignin biosynthesis, bind the nucleotide binding leucine-rich repeat Rp1 proteins to modulate the defense response. Plant Physiology 169(3):2230-2243.

Weng JK, Chapple C (2010). The origin and evolution of lignin biosynthesis. New Phytologist 187(2):273-285. https://doi.org/10.1111/j.1469-8137.2010.03327.x

Wu J, Wang Z, Shi Z, Zhang S, Ming R, Zhu S, Khan MA, Tao S, Korban SS, Wang H (2013). The genome of the pear (Pyrus bretschneideri Rehd.). Genome Research 23(2):396-408. https://doi.org/10.1101/gr.144311.112

Xu Z, Zhang D, Hu J, Zhou X, Ye X, Reichel KL, … Gao P (2009). Comparative genome analysis of lignin biosynthesis gene families across the plant kingdom. BMC Bioinformatics 10(11):1-15. https://doi.org/10.1186/1471-2105-10-S11-S3

Ye SY, Gao WY (2008). Hydroxysafflor yellow A protects neuron against hypoxia injury and suppresses inflammatory responses following focal ischemia reperfusion in rats. Archives of Pharmacal Research 31(8):1010-1015. https://doi.org/10.1007/s12272-001-1261-y

Zhang Y, Guo J, Dong H, Zhao X, Zhou L, Li X, Liu J, Niu Y (2011). Hydroxysafflor yellow A protects against chronic carbon tetrachloride-induced liver fibrosis. European Journal of Pharmacology 660(2-3):438-444. https://doi.org/10.1016/j.ejphar.2011.04.015