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

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.

Keywords

Phoebe bournei / Hsf gene family / Evolutionary analysis / Expression mechanism / Abiotic stresses

References

[1]	Ali A, Petrov V, Yun DJ, Gechev T (2023) Revisiting plant salt tolerance: novel components of the SOS pathway. Trends Plant Sci 28(9):1060–1069. https://doi.org/10.1016/j.tplants.2023.04.003
[2]	Andrási N, Pettkó-Szandtner A, Szabados L (2020) Diversity of plant heat shock factors: regulation, interactions, and functions. J Exp Bot 72(5):1558–1575
[3]	Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME Suite: tools for motif discovery and searching. Nucleic Acids Res 37(suppl_2):W202–W208
[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 (2022) Current status and trends in forest genomics. For Res 2:11. https://doi.org/10.48130/FR-2022-0011
[5]	Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4(1):10
[6]	Chen CJ, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R (2020a) TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant 13(8):1194–1202
[7]	Chen K, Li GJ, Bressan RA, Song CP, Zhu JK, Zhao Y (2020b) Abscisic acid dynamics, signaling, and functions in plants. J Integr Plant Biol 62(1):25–54
[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 (2020c) The Phoebe genome sheds light on the evolution of magnoliids. Hortic Res 7(1):146
[9]	Chen CJ, Wu Y, Xia R (2022) A painless way to customize Circos plot: From data preparation to visualization using TBtools. iMeta 1(3):35
[10]	Chidambaranathan P, Jagannadham PTK, Satheesh V, Kohli D, Basavarajappa SH, Chellapilla B, Kumar J, Jain PK, Srinivasan R (2018) Genome-wide analysis identifies chickpea (Cicer arietinum) heat stress transcription factors (Hsfs) responsive to heat stress at the pod development stage. J Plant Res 131(3):525–542
[11]	de Medeiros RLS, de Paula RC, de Souza JVO, Pedro J (2023) Abiotic stress on seed germination and plant growth of Zeyheria tuberculosa. J For Res. https://doi.org/10.1007/s11676-023-01608-3
[12]	Ding YJ, Zhang JH, Lu YF, Ep L, Lou LH, Tong ZK (2015) Development of EST-SSR markers and analysis of genetic diversity in natural populations of endemic and endangered plant Phoebe chekiangensis. Biochem Syst Ecol 63:183–189
[13]	Ding X, Xiao JH, Li L, Conran JG, Li J (2019) Congruent species delimitation of two controversial gold-thread nanmu tree species based on morphological and restriction site-associated DNA sequencing data. J Syst Evol 57(3):234–246
[14]	Doring P, Treuter E, Kistner C, Lyck R, Chen A, Nover L (2000) The role of AHA motifs in the activator function of tomato heat stress transcription factors HsfA1 and HsfA2. Plant Cell 12(2):265–278
[15]	Dossa K, Diouf D, Cissé N (2016) Genome-wide investigation of Hsf genes in Sesame reveals their segmental duplication expansion and their active role in drought stress response. Front Plant Sci 7:1522
[16]	Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797
[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 (2018) The Pfam protein families database in 2019. Nucleic Acids Res 47(D1):D427–D432. https://doi.org/10.1093/nar/gky995
[18]	Giorno F, Guerriero G, Baric S, Mariani C (2012) Heat shock transcriptional factors in Malus domestica: identification, classification and expression analysis. BMC Genomics 13(1):639
[19]	Guo M, Liu JH, Ma X, Luo DX, Gong ZH, Lu MH (2016) The plant heat stress transcription factors (HSFs): Structure, regulation, and function in response to abiotic stresses. Front Plant Sci 7:114
[20]	Guo Q, Jiang JH, Yao WJ, Li L, Zhao K, Cheng ZH, Han LB, Wei R, Zhou BR, Jiang TB (2021) Genome-wide analysis of poplar HD-zip family and over-expression of PsnHDZ63 confers salt tolerance in transgenic Populus simonii × P. nigra. Plant Sci 311:111021. https://doi.org/10.1016/j.plantsci.2021.111021
[21]	Guo Q, Wei R, Xu M, Yao WJ, Jiang JH, Ma XJ, Qu GZ, Jiang TB (2023) Genome-wide analysis of HSF family and overexpression of PsnHSF21 confers salt tolerance in Populus simonii×P. nigra. Front Plant Sci 14:1160102
[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 (2022) The chromosome-scale genome of Phoebe bournei reveals contrasting fates of terpene synthase (TPS)-a and TPS-b subfamilies. Plant Commun 3(6):100410
[23]	Holub EB (2001) The arms race is ancient history in Arabidopsis, the wildflower. Nat Rev Genet 2:516–527
[24]	Horton P, Park KJ, Obayashi T, Fujita N, Harada H, Adams-Collier CJ, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35(suppl_2):W585–W587
[25]	Hu Y, Han YT, Wei W, Li YJ, Zhang K, Gao YR, Zhao FL, Feng JY (2015) Identification, isolation, and expression analysis of heat shock transcription factors in the diploid woodland strawberry Fragaria vesca. Front Plant Sci 6:736
[26]	Huang YC, Niu CY, Yang CR, Jinn TL (2016) The heat stress factor HSFA6b connects ABA signaling and ABA-mediated heat responses. Plant Physiol 172(2):1182–1199
[27]	Ibraheem O, Botha CEJ, Bradley G (2010) 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 34(5):268–283
[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 (2022) 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 4(6):696–709
[29]	Jin JP, Tian F, Yang DC, Meng YQ, Kong L, Luo JC, Gao G (2017) PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res 45(D1):D1040–D1045
[30]	Kerchev P, van der Meer T, Sujeeth N, Verlee A, Stevens CV, Van Breusegem F, Gechev T (2020) Molecular priming as an approach to induce tolerance against abiotic and oxidative stresses in crop plants. Biotechnol Adv 40:107503
[31]	Kotak S, Port M, Ganguli A, Bicker F, Von Koskull-D?ring P (2004) 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 39(1):98–112
[32]	Kowalczewski P?, Radzikowska D, Ivani?ová E, Szwengiel A, Ka?ániová M, Sawinska Z (2020) Influence of abiotic stress factors on the antioxidant properties and polyphenols profile composition of green barley (Hordeum vulgare L.). Int J Mol Sci 21(2):397
[33]	Le Hir H, Nott A, Moore MJ (2003) How introns influence and enhance eukaryotic gene expression. Trends Biochem Sci 28(4):215–220
[34]	Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S (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(1):325–327
[35]	Letunic I, Bork P (2021) Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 49(W1):W293–W296
[36]	Li YG, Liu XH, Ma JW, Zhang XM, Xu LA (2018) Phenotypic variation in Phoebe bournei populations preserved in the primary distribution area. J Forestry Res 29:35–44
[37]	Li X, Liu LL, Sun SX, Li YM, Jia L, Ye SL, Yu YX, Dossa K, Luan YP (2022) Leaf-transcriptome profiles of phoebe bournei provide insights into temporal drought stress responses. Front Plant Sci 13:1010314
[38]	Lin YX, Jiang HY, Chu ZX, Tang XL, Zhu SW, Cheng BJ (2011) Genome-wide identification, classification and analysis of heat shock transcription factor family in maize. BMC Genomics 12(1):76
[39]	Lin Q, Jiang Q, Lin JY, Wang DL, Li SJ, Liu CR, Sun CD, Chen KS (2015) Heat shock transcription factors expression during fruit development and under hot air stress in Ponkan (Citrus reticulata Blanco cv. Ponkan) fruit. Gene 559(2):129–136
[40]	Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25(4):402–408
[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 (2016) CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res 45(D1):D200–D203
[42]	Mittal D, Chakrabarti S, Sarkar A, Singh A, Grover A (2009) 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 47(9):785–795
[43]	Nishizawa A, Yabuta Y, Yoshida E, Maruta T, Yoshimura K, Shigeoka S (2006) Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant J 48(4):535–547
[44]	Nover L, Bharti K, D?ring P, Mishra S, Ganguli A, Scharf KD (2001) Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need? Cell Stress Chaperones 6(3):177–189
[45]	Penfield S (2008) Temperature perception and signal transduction in plants. New Phytol 179(3):615–628
[46]	Polle A, Chen S (2015) On the salty side of life: molecular, physiological and anatomical adaptation and acclimation of trees to extreme habitats. Plant Cell Environ 38:1794–1816
[47]	Prieto-Dapena P, Almoguera C, Personat JM, Merchan F, Jordano J (2017) Seed-specific transcription factor HSFA9 links late embryogenesis and early photomorphogenesis. J Exp Bot 68(5):1097–1108
[48]	Ratheesh Kumar R, Nagarajan NS, Arunraj SP, Devanjan S, Rajan VBV, Esthaki VK, D’Silva P (2012) HSPIR: a manually annotated heat shock protein information resource. Bioinformatics 28(21):2853–2855
[49]	Sakurai H, Enoki Y (2010) Novel aspects of heat shock factors: DNA recognition, chromatin modulation and gene expression. FEBS J 277(20):4140–4149
[50]	Scharf KD, Rose S, Zott W, Sch?ffl F, Nover L, Sch?ff F (1990) 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 9(13):4495–4501
[51]	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 2:104–119
[52]	Shaul O (2017) How introns enhance gene expression. Int J Biochem Cell Biol 91:145–155
[53]	Sun TP (2011) The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants. Curr Biol 21(9):R338–R345
[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 (2021) Genome-wide identification of HSF family in peach and functional analysis of PpHSF5 involvement in root and aerial organ development. PeerJ 9:e10961
[55]	von Koskull-D?ring P, Scharf K-D, Nover L (2007) The diversity of plant heat stress transcription factors. Trends Plant Sci 12(10):452–457
[56]	Wang XM, Shi X, Chen SY, Ma C, Xu SB (2018) Evolutionary origin, gradual accumulation and functional divergence of heat shock factor gene family with plant evolution. Front Plant Sci 9:71
[57]	Wang LL, Liu YH, Chai MN, Chen HH, Aslam M, Niu XP, Qin Y, Cai HY (2021) Genome-wide identification, classification, and expression analysis of the HSF gene family in pineapple (Ananas comosus). PeerJ 9:e11329
[58]	Wang LL, Liu YH, Chai GF, Zhang D, Fang YY, Deng K, Aslam M, Niu XP, Zhang WB, Qin Y, Wang XM (2023) Identification of passion fruit HSF gene family and the functional analysis of PeHSF-C1a in response to heat and osmotic stress. Plant Physiol Biochem 200:107800
[59]	Waterhouse AM, Procter JB, Martin DMA, Clamp M, Barton GJ (2009) Jalview Version-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25(9):1189–1191
[60]	Yang ZJ, Wu XH, Grossnickle SC, Chen LH, Yu XX, El-Kassaby YA, Feng JL (2020) Formula fertilization promotes Phoebe bournei robust seedling cultivation. Forests 11(7):781
[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 (2022) Large-scale analyses of heat shock transcription factors and database construction based on whole-genome genes in horticultural and representative plants. Hortic Res. https://doi.org/10.1093/hr/uhac035
[62]	Yuan T, Liang JX, Dai JH, Zhou XR, Liao WH, Guo ML, Aslam M, Li SB, Cao GQ, Cao SJ (2022) Genome-wide identification of Eucalyptus heat shock transcription factor family and their transcriptional analysis under salt and temperature stresses. Int J Mol Sci 23(14):8044
[63]	Zhang J, Liu BB, Li JB, Zhang L, Wang Y, Zheng HQ, Lu MZ, Chen J (2015) Hsf and Hsp gene families in Populus: genome-wide identification, organization and correlated expression during development and in stress responses. BMC Genomics 16(1):181
[64]	Zhang JH, Zhu YJ, Pan Y, Huang HH, Li CL, Li GZ, Tong ZK (2018) Transcriptomic profiling and identification of candidate genes in two Phoebe bournei ecotypes with contrasting cold stress responses. Trees 32(5):1315–1333
[65]	Zhang HM, Zhu JH, Gong ZZ, Zhu JK (2022a) Abiotic stress responses in plants. Nat Rev Genet 23(2):104–119
[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 (2022b) 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 22(1):33
[67]	Zhao K, Dang H, Zhou LD, Hu J, Jin X, Han YZ, Wang SJ (2023) Genome-wide identification and expression analysis of the HSF gene family in Poplar. Forests 14(3):510
[68]	Zupanska AK, LeFrois C, Ferl RJ, Paul AL (2019) HSFA2 functions in the physiological adaptation of undifferentiated plant cells to spaceflight. Int J Mol Sci 20(2):390