Genome wide investigation of Hsf gene family in Phoebe bournei: identification, evolution, and expression after abiotic stresses

doi:10.1007/s11676-023-01661-y

Abstract

Abstract:

Heat shock transcription factors (Hsfs) have important roles during plant growth and development and responses to abiotic stresses. The identification and function of Hsf genes have been thoroughly studied in various herbaceous plant species, but not woody species, especially Phoebe bournei, an endangered, unique species in China. In this study, 17 members of the Hsf gene family were identified from P. bournei using bioinformatic methods. Phylogenetic analysis indicated that PbHsf genes were grouped into three subfamilies: A, B, and C. Conserved motifs, three-dimensional structure, and physicochemical properties of the PbHsf proteins were also analyzed. The structure of the PbHsf genes varied in the number of exons and introns. Prediction of cis-acting elements in the promoter region indicated that PbHsf genes are likely involved in responses to plant hormones and stresses. A collinearity analysis demonstrated that expansions of the PbHsf gene family mainly take place via segmental duplication. The expression levels of PbHsf genes varied across different plant tissues. On the basis of the expression profiles of five representative PbHsf genes during heat, cold, salt, and drought stress, PbHsf proteins seem to have multiple functions depending on the type of abiotic stress. This systematic, genome-wide investigation of PbHsf genes in P. bournei and their expression patterns provides valuable insights and information for further functional dissection of Hsf proteins in this endangered, unique species.

Key words: Phoebe bournei, Hsf gene family, Evolutionary analysis, Expression mechanism, Abiotic stresses

Wenhai Liao, Xinghao Tang, Jingshu Li, Qiumian Zheng, Ting Wang, Shengze Cheng, Shiping Chen, Shijiang Cao, Guangqiu Cao. Genome wide investigation of Hsf gene family in Phoebe bournei: identification, evolution, and expression after abiotic stresses[J]. JOURNAL OF FORESTRY RESEARCH, 2024, 35(1): 11-.

Wenhai Liao, Xinghao Tang, Jingshu Li, Qiumian Zheng, Ting Wang, Shengze Cheng, Shiping Chen, Shijiang Cao, Guangqiu Cao. [J]. 林业研究(英文版), 2024, 35(1): 11-.

References 68

1	Ali A, Petrov V, Yun DJ, Gechev T. Revisiting plant salt tolerance: novel components of the SOS pathway. Trends Plant Sci, 2023, 28(9): 1060-1069, DOI
2	Andrási N, Pettkó-Szandtner A, Szabados L. Diversity of plant heat shock factors: regulation, interactions, and functions. J Exp Bot, 2020, 72(5): 1558-1575, DOI
3	Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS. MEME Suite: tools for motif discovery and searching. Nucleic Acids Res, 2009, 37(suppl_2): W202-W208, DOI
4	Borthakur D, Busov V, Cao XH, Du QZ, Gailing O, Isik F, Ko JH, Li CH, Li QZ, Niu SH, Qu GZ, Vu THG, Wang XR, Wei ZG, Zhang L, Wei HR. Current status and trends in forest genomics. For Res, 2022, 2: 11, DOI
5	Cannon SB, Mitra A, Baumgarten A, Young ND, May G. The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol, 2004, 4(1): 10, DOI
6	Chen CJ, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant, 2020, 13(8): 1194-1202, DOI
7	Chen K, Li GJ, Bressan RA, Song CP, Zhu JK, Zhao Y. Abscisic acid dynamics, signaling, and functions in plants. J Integr Plant Biol, 2020, 62(1): 25-54, DOI
8	Chen SP, Sun WH, Xiong YF, Jiang YT, Liu XD, Liao XY, Zhang DY, Jiang SZ, Li Y, Liu B, Ma L, Yu X, He L, Liu B, Feng JL, Feng LZ, Wang ZW, Zou SQ, Lan SR, Liu ZJ. The Phoebe genome sheds light on the evolution of magnoliids. Hortic Res, 2020, 7(1): 146, DOI
9	Chen CJ, Wu Y, Xia R. A painless way to customize Circos plot: From data preparation to visualization using TBtools. iMeta, 2022, 1(3): 35, DOI
10	Chidambaranathan P, Jagannadham PTK, Satheesh V, Kohli D, Basavarajappa SH, Chellapilla B, Kumar J, Jain PK, Srinivasan R. Genome-wide analysis identifies chickpea (Cicer arietinum) heat stress transcription factors (Hsfs) responsive to heat stress at the pod development stage. J Plant Res, 2018, 131(3): 525-542, DOI
11	de Medeiros RLS, de Paula RC, de Souza JVO, Pedro J. Abiotic stress on seed germination and plant growth of Zeyheria tuberculosa. J For Res, 2023, DOI
12	Ding YJ, Zhang JH, Lu YF, Ep L, Lou LH, Tong ZK. Development of EST-SSR markers and analysis of genetic diversity in natural populations of endemic and endangered plant Phoebe chekiangensis. Biochem Syst Ecol, 2015, 63: 183-189, DOI
13	Ding X, Xiao JH, Li L, Conran JG, Li J. Congruent species delimitation of two controversial gold-thread nanmu tree species based on morphological and restriction site-associated DNA sequencing data. J Syst Evol, 2019, 57(3): 234-246, DOI
14	Doring P, Treuter E, Kistner C, Lyck R, Chen A, Nover L. The role of AHA motifs in the activator function of tomato heat stress transcription factors HsfA1 and HsfA2. Plant Cell, 2000, 12(2): 265-278, DOI
15	Dossa K, Diouf D, Cissé N. Genome-wide investigation of Hsf genes in Sesame reveals their segmental duplication expansion and their active role in drought stress response. Front Plant Sci, 2016, 7: 1522, DOI
16	Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res, 2004, 32(5): 1792-1797, DOI
17	El-Gebali S, Mistry J, Bateman A, Eddy SR, Luciani A, Potter SC, Qureshi M, Richardson LJ, Salazar GA, Smart A, Sonnhammer ELL, Hirsh L, Paladin L, Piovesan D, Tosatto SCE, Finn RD. The Pfam protein families database in 2019. Nucleic Acids Res, 2018, 47(D1): D427-D432, DOI
18	Giorno F, Guerriero G, Baric S, Mariani C. Heat shock transcriptional factors in Malus domestica: identification, classification and expression analysis. BMC Genomics, 2012, 13(1): 639, DOI
19	Guo M, Liu JH, Ma X, Luo DX, Gong ZH, Lu MH. The plant heat stress transcription factors (HSFs): Structure, regulation, and function in response to abiotic stresses. Front Plant Sci, 2016, 7: 114, DOI
20	Guo Q, Jiang JH, Yao WJ, Li L, Zhao K, Cheng ZH, Han LB, Wei R, Zhou BR, Jiang TB. Genome-wide analysis of poplar HD-zip family and over-expression of PsnHDZ63 confers salt tolerance in transgenic Populus simonii × P. nigra. Plant Sci, 2021, 311: 111021, DOI
21	Guo Q, Wei R, Xu M, Yao WJ, Jiang JH, Ma XJ, Qu GZ, Jiang TB. Genome-wide analysis of HSF family and overexpression of PsnHSF21 confers salt tolerance in Populus simonii×P. nigra. Front Plant Sci, 2023, 14: 1160102, DOI
22	Han X, Zhang JH, Han S, Chong SL, Meng GL, Song MY, Wang Y, Zhou SC, Liu CC, Lou LH, Lou XZ, Cheng LJ, Lin E, Huang HH, Yang Q, Tong ZK. The chromosome-scale genome of Phoebe bournei reveals contrasting fates of terpene synthase (TPS)-a and TPS-b subfamilies. Plant Commun, 2022, 3(6): 100410, DOI
23	Holub EB. The arms race is ancient history in Arabidopsis, the wildflower. Nat Rev Genet, 2001, 2: 516-527, DOI
24	Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K. WoLF PSORT: protein localization predictor. Nucleic Acids Res, 2007, 35(suppl_2): W585-W587, DOI
25	Hu Y, Han YT, Wei W, Li YJ, Zhang K, Gao YR, Zhao FL, Feng JY. Identification, isolation, and expression analysis of heat shock transcription factors in the diploid woodland strawberry Fragaria vesca. Front Plant Sci, 2015, 6: 736, DOI
26	Huang YC, Niu CY, Yang CR, Jinn TL. The heat stress factor HSFA6b connects ABA signaling and ABA-mediated heat responses. Plant Physiol, 2016, 172(2): 1182-1199
27	Ibraheem O, Botha CEJ, Bradley G. In silico analysis of cis-acting regulatory elements in 5’ regulatory regions of sucrose transporter gene families in rice (Oryza sativa Japonica) and Arabidopsis thaliana. Comput Biol Chem, 2010, 34(5): 268-283, DOI
28	Jiao LC, Lu Y, Zhang M, Chen YP, Wang ZS, Guo Y, Xu C, Guo J, He T, Ma LY, Gao WQ, Wang J, Zhou SL, Zhang YG, Jiang XM, Baas P, Yin YF. Ancient plastid genomes solve the tree species mystery of the imperial wood “Nanmu” in the Forbidden City, the largest existing wooden palace complex in the world. Plants People Planet, 2022, 4(6): 696-709, DOI
29	Jin JP, Tian F, Yang DC, Meng YQ, Kong L, Luo JC, Gao G. PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res, 2017, 45(D1): D1040-D1045, DOI
30	Kerchev P, van der Meer T, Sujeeth N, Verlee A, Stevens CV, Van Breusegem F, Gechev T. Molecular priming as an approach to induce tolerance against abiotic and oxidative stresses in crop plants. Biotechnol Adv, 2020, 40, DOI
31	Kotak S, Port M, Ganguli A, Bicker F, Von Koskull-Döring P. Characterization of C-terminal domains of Arabidopsis heat stress transcription factors (Hsfs) and identification of a new signature combination of plant class A Hsfs with AHA and NES motifs essential for activator function and intracellular localization. Plant J, 2004, 39(1): 98-112, DOI
32	Kowalczewski PŁ, Radzikowska D, Ivanišová E, Szwengiel A, Kačániová M, Sawinska Z. Influence of abiotic stress factors on the antioxidant properties and polyphenols profile composition of green barley (Hordeum vulgare L.). Int J Mol Sci, 2020, 21(2): 397, DOI
33	Le Hir H, Nott A, Moore MJ. How introns influence and enhance eukaryotic gene expression. Trends Biochem Sci, 2003, 28(4): 215-220, DOI
34	Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res, 2002, 30(1): 325-327, DOI
35	Letunic I, Bork P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res, 2021, 49(W1): W293-W296, DOI
36	Li YG, Liu XH, Ma JW, Zhang XM, Xu LA. Phenotypic variation in Phoebe bournei populations preserved in the primary distribution area. J Forestry Res, 2018, 29: 35-44, DOI
37	Li X, Liu LL, Sun SX, Li YM, Jia L, Ye SL, Yu YX, Dossa K, Luan YP. Leaf-transcriptome profiles of phoebe bournei provide insights into temporal drought stress responses. Front Plant Sci, 2022, 13: 1010314, DOI
38	Lin YX, Jiang HY, Chu ZX, Tang XL, Zhu SW, Cheng BJ. Genome-wide identification, classification and analysis of heat shock transcription factor family in maize. BMC Genomics, 2011, 12(1): 76, DOI
39	Lin Q, Jiang Q, Lin JY, Wang DL, Li SJ, Liu CR, Sun CD, Chen KS. Heat shock transcription factors expression during fruit development and under hot air stress in Ponkan (Citrus reticulata Blanco cv. Ponkan) fruit. Gene, 2015, 559(2): 129-136, DOI
40	Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods, 2001, 25(4): 402-408, DOI
41	Marchler-Bauer A, Bo Y, Han LY, He JE, Lanczycki CJ, Lu SN, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Lu F, Marchler GH, Song JS, Thanki N, Wang ZX, Yamashita RA, Zhang DC, Zheng CJ, Geer LY, Bryant SH. CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res, 2016, 45(D1): D200-D203, DOI
42	Mittal D, Chakrabarti S, Sarkar A, Singh A, Grover A. Heat shock factor gene family in rice: genomic organization and transcript expression profiling in response to high temperature, low temperature and oxidative stresses. Plant Physiol Biochem, 2009, 47(9): 785-795, DOI
43	Nishizawa A, Yabuta Y, Yoshida E, Maruta T, Yoshimura K, Shigeoka S. Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant J, 2006, 48(4): 535-547, DOI
44	Nover L, Bharti K, Döring P, Mishra S, Ganguli A, Scharf KD. Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need?. Cell Stress Chaperones, 2001, 6(3): 177-189, DOI
45	Penfield S. Temperature perception and signal transduction in plants. New Phytol, 2008, 179(3): 615-628, DOI
46	Polle A, Chen S. On the salty side of life: molecular, physiological and anatomical adaptation and acclimation of trees to extreme habitats. Plant Cell Environ, 2015, 38: 1794-1816, DOI
47	Prieto-Dapena P, Almoguera C, Personat JM, Merchan F, Jordano J. Seed-specific transcription factor HSFA9 links late embryogenesis and early photomorphogenesis. J Exp Bot, 2017, 68(5): 1097-1108, DOI
48	Ratheesh Kumar R, Nagarajan NS, Arunraj SP, Devanjan S, Rajan VBV, Esthaki VK, D’Silva P. HSPIR: a manually annotated heat shock protein information resource. Bioinformatics, 2012, 28(21): 2853-2855, DOI
49	Sakurai H, Enoki Y. Novel aspects of heat shock factors: DNA recognition, chromatin modulation and gene expression. FEBS J, 2010, 277(20): 4140-4149, DOI
51	Scharf KD, Rose S, Zott W, Schöffl F, Nover L, Schöff F. Three tomato genes code for heat stress transcription factors with a region of remarkable homology to the DNA-binding domain of the yeast HSF. EMBO J, 1990, 9(13): 4495-4501, DOI
50	Scharf KD, Berberich T, Ebersberger I. Nover L (2012) The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biophys Acta Gene Regul Mech, 1819, 2: 104-119
52	Shaul O. How introns enhance gene expression. Int J Biochem Cell Biol, 2017, 91: 145-155, DOI
53	Sun TP. The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants. Curr Biol, 2011, 21(9): R338-R345, DOI
54	Tan B, Yan L, Li HN, Lian XD, Cheng J, Wang W, Zheng XB, Wang XB, Li JD, Ye X, Zhang LL, Li ZQ, Feng JC. Genome-wide identification of HSF family in peach and functional analysis of PpHSF5 involvement in root and aerial organ development. PeerJ, 2021, 9, DOI
55	von Koskull-Döring P, Scharf K-D, Nover L. The diversity of plant heat stress transcription factors. Trends Plant Sci, 2007, 12(10): 452-457, DOI
56	Wang XM, Shi X, Chen SY, Ma C, Xu SB. Evolutionary origin, gradual accumulation and functional divergence of heat shock factor gene family with plant evolution. Front Plant Sci, 2018, 9: 71, DOI
57	Wang LL, Liu YH, Chai MN, Chen HH, Aslam M, Niu XP, Qin Y, Cai HY. Genome-wide identification, classification, and expression analysis of the HSF gene family in pineapple (Ananas comosus). PeerJ, 2021, 9, DOI
58	Wang LL, Liu YH, Chai GF, Zhang D, Fang YY, Deng K, Aslam M, Niu XP, Zhang WB, Qin Y, Wang XM. Identification of passion fruit HSF gene family and the functional analysis of PeHSF-C1a in response to heat and osmotic stress. Plant Physiol Biochem, 2023, 200, DOI
59	Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ. Jalview Version-a multiple sequence alignment editor and analysis workbench. Bioinformatics, 2009, 25(9): 1189-1191, DOI
60	Yang ZJ, Wu XH, Grossnickle SC, Chen LH, Yu XX, El-Kassaby YA, Feng JL. Formula fertilization promotes Phoebe bournei robust seedling cultivation. Forests, 2020, 11(7): 781, DOI
61	Yu T, Bai Y, Liu Z, Wang ZY, Yang QH, Wu T, Feng SY, Zhang Y, Shen SQ, Li Q, Gu LQ, Song XM. Large-scale analyses of heat shock transcription factors and database construction based on whole-genome genes in horticultural and representative plants. Hortic Res, 2022, DOI
62	Yuan T, Liang JX, Dai JH, Zhou XR, Liao WH, Guo ML, Aslam M, Li SB, Cao GQ, Cao SJ. Genome-wide identification of Eucalyptus heat shock transcription factor family and their transcriptional analysis under salt and temperature stresses. Int J Mol Sci, 2022, 23(14): 8044, DOI
63	Zhang J, Liu BB, Li JB, Zhang L, Wang Y, Zheng HQ, Lu MZ, Chen J. Hsf and Hsp gene families in Populus: genome-wide identification, organization and correlated expression during development and in stress responses. BMC Genomics, 2015, 16(1): 181, DOI
64	Zhang JH, Zhu YJ, Pan Y, Huang HH, Li CL, Li GZ, Tong ZK. Transcriptomic profiling and identification of candidate genes in two Phoebe bournei ecotypes with contrasting cold stress responses. Trees, 2018, 32(5): 1315-1333, DOI
65	Zhang HM, Zhu JH, Gong ZZ, Zhu JK. Abiotic stress responses in plants. Nat Rev Genet, 2022, 23(2): 104-119, DOI
66	Zhang Q, Geng J, Du YL, Zhao Q, Zhang WJ, Fang QX, Yin ZG, Li JH, Yuan XK, Fan YR, Cheng X, Du JD. Heat shock transcription factor (Hsf) gene family in common bean (Phaseolus vulgaris): genome-wide identification, phylogeny, evolutionary expansion and expression analyses at the sprout stage under abiotic stress. BMC Plant Biol, 2022, 22(1): 33, DOI
67	Zhao K, Dang H, Zhou LD, Hu J, Jin X, Han YZ, Wang SJ. Genome-wide identification and expression analysis of the HSF gene family in Poplar. Forests, 2023, 14(3): 510, DOI
68	Zupanska AK, LeFrois C, Ferl RJ, Paul AL. HSFA2 functions in the physiological adaptation of undifferentiated plant cells to spaceflight. Int J Mol Sci, 2019, 20(2): 390, DOI