Bioinformatics and stress response expression analysis of poplar HSF family genes
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摘要:目的 探究小黑杨热激转录因子HSF在应答高温和高盐胁迫时发挥的关键作用。保守结构域和顺式作用元件预测等对杨树HSF转录因子家族基因进行生物信息学分析。本研究以小黑杨为材料，经过37 ℃高温胁迫半个月后观察其形态变化；将小黑杨在37 ℃下分别处理0、12、24、48 h，采用RT-qPCR对小黑杨组织中的PsnHSFs基因进行时空表达分析；将小黑杨于150 mmol/L NaCl胁迫分别处理0、24 h，通过RNA-seq分析PsnHSFs基因的相对表达量变化，并通过RT-qPCR进行验证。结果 通过结构特征和系统发育比较将29个HSF转录因子家族基因分成A、B和C三个亚家族，各亚家族分别包含18、10和1个HSF基因；HSF编码的氨基酸序列长度介于209 ~ 595之间，均为亲水性蛋白；其N端具有高度保守的DBD结构域，由三个保守基序构成；HSF基因启动子序列中包含DRE core、ABRE和TC-rich等多种顺式作用元件。小黑杨经37 ℃高温处理后其株高仅为对照的76.51%，叶片呈卷曲状，叶表面粗糙，叶面积显著减小且苗干多侧枝柔软无韧性。RT-qPCR与RNA-seq结果表明，PsnHSFs被高温、高盐胁迫诱导表达。高温处理后其株高仅为对照的76.51%，叶片呈卷曲状，叶表面粗糙，叶面积显著减小且苗干多侧枝柔软无韧性。RT-qPCR与RNA-seq结果表明，PsnHSFs被高温、高盐胁迫诱导表达。家族基因以及揭示HSF参与木本植物胁迫应答的分子机制调控具有参考意义。Abstract:Objective This paper aims to investigate the key role of heat shock transcription factor HSF of Populus simonii × P. nigra in response to high temperature and high salt stress.Method Bioinformatics analysis of poplar HSF transcription factor family genes was carried out through multi-sequence alignment, phylogenetic tree construction, analysis of protein physicochemical properties, conserved domains and cis-acting element prediction. In this study, P. simonii × P. nigra was used as a material, and its morphological changes were observed after 37 ℃ high temperature treatment for half a month and the PsnHSFs genes were analyzed for spatio-temporal expression after 37 ℃ high temperature treatment for 0, 12, 24 and 48 h. In addition, P. simonii × P. nigra seedlings were used for 150 mM NaCl stress treatment for 0 and 24 h, the relative expression level of PsnHSFs was analyzed by RNA-seq and verified by RT-qPCR.Result The 29 HSF genes were divided into three subfamilies of A, B and C by structural characteristics and phylogenetic comparison, each subfamily contained 18, 10 and 1 genes. The sequence length of amino acid HSF encoding was between 209 and 595. The HSF proteins were hydrophilic proteins; the N-terminal had a highly conserved DBD domain composed of three conserved motifs. The promoter sequences of the HSF genes contained a variety of cis-acting elements such as DRE core, ABRE and TC-rich elements. After high temperature treatment, the plant height was only 76.51% of control. The leaf was curled and rough, the leaf area was significantly reduced, and the trees had multiple branches which were soft and inflexible. RT-qPCR and RNA-seq results showed that PsnHSFs were induced by high temperature and high salt stress.Conclusion The growth and development of poplar was significantly affected by high temperature, the PsnHSFs genes of poplar play an important role in response to high temperature and high salt stress. This study provides a reference for understanding the HSF family genes in poplar and revealing the molecular mechanism of HSF involved in stress response in woody plants.
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Keywords:
- Populus simonii × P. nigra /
- PsnHSFs /
- bioinformatics /
- stress response
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图 1 杨树与拟南芥HSF家族基因系统进化树
Figure 1. Phylogenetic tree of HSF family in poplar and Arabidopsis thaliana
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图 2 PtrHSFs结构域分析
A. 杨树PtrHSFs基本结构图；B. 杨树PtrHSFs中DBD保守结构域；C. 杨树PtrHSFs氨基酸序列20个保守基序。A, basic structure of PtrHSFs of poplar; B, DBD conservative domain in PtrHSFs of poplar; C, there are 20 conserved amino acid sequences of PtrHSFs in poplar.
Figure 2. PtrHSFs domain analysis
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图 3 小黑杨高温胁迫生长状态
A. 小黑杨非胁迫和胁迫生长状态；a为对照，b、c、d为37 ℃高温处理小黑杨；B. 小黑杨对照和高温胁迫处理半个月的株高。数据均为平均值 ± 标准差；星号表示胁迫处理植株与非胁迫处理植株之间的差异性，*、**、***分别表示在P < 0.05、P < 0.01、P < 0.001水平上差异显著。下同。A, non-stress and stress growth state of P. simonii × P. nigra; a, control; b, c, d, P. simonii × P. nigra trees under 37 ℃ high temperature treatment; B, plant height of P. simonii × P. nigra under control and HT for half a month. The data annotation in the picture is average value ± SD; the asterisk indicates that the difference between stressed and non-stressed plants. *, **, *** indicate significant difference at P < 0.05, P < 0.01, P < 0.001 level, respectively. The same below.
Figure 3. Growth state of P. simonii × P. nigra under high temperature stress
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图 4 小黑杨高温胁迫叶片状态
A.形态学上端向下第3片到第11片小黑杨叶片；B.小黑杨第6片叶表面；a.对照；b、c、d. 37 ℃高温处理小黑杨。A, the 3rd to 11th leaves of P. simonii × P. nigra from apical side; B, surface of the 6th leaf of P. simonii × P. nigra; a, control; b, c, d, P. simonii × P. nigra under 37 ℃ high temperature treatment.
Figure 4. Leaf state of P. simonii × P. nigra under high temperature stress
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图 5 小黑杨PsnHSFs转录因子基因高温胁迫下相对表达量
Figure 5. Relative expression level of PsnHSFs transcription factor genes in P. simonii × P. nigra under high temperature stress
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图 6 小黑杨PsnHSFs应答盐胁迫热谱图分析
C1 ~ C4. 对照组的4个生物学重复；N1 ~ N4. 处理组的4个生物学重复。C1−C4, four biological repeats in control; N1−N4, four biological repeats in treatment group.
Figure 6. Thermogram analysis of PsnHSFs genes responsing to salt stress of P. simonii × P. nigra
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图 7 小黑杨PsnHSFs基因应答盐胁迫定量分析
Figure 7. Quantitative analysis of PsnHSFs genes responsing to salt stress in P. simonii × P. nigra
表 1 小黑杨PsnHSFs转录因子基因定量引物
Table 1 Quantitative primers for PsnHSFs transcription factor genes of Populus simonii × P. nigra
基因名称 Gene name 基因编号 Gene ID 正向引物(5′—3′) Forward primer (5′−3′) 反向引物(3′—5′) Reverse primer (3′−5′) PsnHSF1 Potri.001G108100.1 CTACGATGGCGGCATCAGCTG CAGCTGATGCCGCCATCGTAG PsnHSF2 Potri.001G138900.1 GCTTAGGACTATCAGTCGGCG CCTCTTAAGCCTCTCTACCTC PsnHSF3 Potri.001G273700.1 CCCAACACCATCACCAGCACT GATTATCTTCTGAGAGTGCAG PsnHSF4 Potri.001G320900.1 CCTACTTTTGTTGAACACCTT TACTGTGATTTTCCACAAGAC PsnHSF5 Potri.002G048200.1 ATGAATCCATATCTAACAGTG GTATCATGTAAACCTTCCATC PsnHSF6 Potri.002G124800.1 CAGCTCAGCCACAAGTAGCCA GTGAATCACACCAGTTGTTGG PsnHSF7 Potri.003G095000.1 GCTTAGGATTATCAGTCGGCG CTTCCTCGAGCCCAAATTTCC PsnHSF8 Potri.004G042600.1 GCGAGCCCAGCACGTTTCCAG CTAGTTCCATTTTCTCTCTTC PsnHSF9 Potri.004G062300.1 GTATCTTTTGTGACCCGAGTG GAAGTCACCGTCTGATTATCC PsnHSF10 Potri.005G214800.1 GATCTAGTAGAGGTGGTGGTG CATACCCTTGCATTTCCAACG PsnHSF11 Potri.006G049200.1 GGACTAACAAGCAACAACCTA CTAGTAAGCTCAGTGCTCAAG PsnHSF12 Potri.006G115700.1 GGAGAGATTGGTTCATCAAGG GTGATGTTTCTCCAATCAGGC PsnHSF13 Potri.006G148200.1 ATGAATACAAGAGAAATGCAG CTTCAACTCATTGAGACTATC PsnHSF14 Potri.006G226800.1 GACATCTCTCACAGACCACAC CTAAGCCTTACAATCTCTGCC PsnHSF15 Potri.007G043800.1 GACAGCGGCTGCGTCTCCGAC GACGTTGACGTGGACCCCAGG PsnHSF16 Potri.008G157600.1 CATCTTCTCAAGAGTATTAGG CTTGCTTGTCTCGCCTTAATC PsnHSF17 Potri.009G068000.1 CAATATCCCAGCACCATCACC CTGAGAGGGCAGTTAGGATAT PsnHSF18 Potri.010G082000.1 CTCCTCAAACTCAGACTTCTC CTTCACTAGTTCCACCATTAG PsnHSF19 Potri.010G104300.1 CTCAGGGCACAGACAATCGAA CTCAACTTCCTTCCAGAGACC PsnHSF20 Potri.011G051600.1 GTGAGCCTAGTATGTTTCCAG CAGTTCAAGTTTCTCTCTTCG PsnHSF21 Potri.011G071700.1 CATACAGCAAACTATAGTGTC GTATAGATAACCAATTCTAGG PsnHSF22 Potri.012G138900.1 GCCATGGTGAAAACGTCGTCG CTCTTCATCTCCGTCAACTCC PsnHSF23 Potri.013G079800.1 CTGTTCATGGTAACCTACCAC TCTAACAAGTTCCTGCATGAG PsnHSF24 Potri.014G027100.1 CAGCTCAGCCACAAGTAGCTA GAGAGATGCTGGTTCTGCTTG PsnHSF25 Potri.014G141400.1 GTTCTCCAATTGCAAACCTGG CAACATGGCACACTTCTTCAC PsnHSF26 Potri.015G141100.1 GTGGCGACGGTGGCGCAAGTG CCGGCGAAGAACTCCTCGTCG PsnHSF27 Potri.016G056500.1 CATGGTCTAGCAAGCAACAAC GTAAGCTCAGTGCTCAAGACC PsnHSF28 Potri.017G059600.1 CTGCTTTTGTTGAACATCTTG AGAACTACAGTGATTTTCGAC PsnHSF29 Potri.T137400.1 CTGAAGAATATAGTTCGCAGG CATAATTATATCTTCATCATC 
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表 2 杨树HSF转录因子基因理化性质
Table 2 Physical and chemical properties of HSF transcription factor genes in poplar
基因名称
Gene name基因编号
Gene ID基因群
Gene
group氨基酸个数
Amino acid
number连锁群
Linkage
group蛋白分子质量
Molecular mass
of protein/Da等电点
Isoelectric
point (PI)脂肪指数
Aliphatic
index (AI)不稳定系数
Instability
index (II)总平均亲水性
Grand average of
hydropathicity
(GRAVY)PtrHSF1 Potri.001G108100.1 B2b 343 Chr01 36 826.6 4.71 69.15 55.66 −0.559 PtrHSF2 Potri.001G138900.1 A1d 595 Chr01 65 369.3 5.51 74.57 64.08 −0.532 PtrHSF3 Potri.001G273700.1 B4d 270 Chr01 31 292.3 7.15 70.37 56.72 −0.610 PtrHSF4 Potri.001G320900.1 A5b 490 Chr01 54 702.7 6.01 70.67 56.61 −0.770 PtrHSF5 Potri.002G048200.1 A7b 359 Chr02 41 148.3 5.13 67.41 57.79 −0.808 PtrHSF6 Potri.002G124800.1 B4a 364 Chr02 40 440.7 8.15 73.90 51.74 −0.468 PtrHSF7 Potri.003G095000.1 A1a 507 Chr03 55 694.9 4.61 70.81 58.55 −0.601 PtrHSF8 Potri.004G042600.1 A1 209 Chr04 24 028.4 9.50 70.53 57.40 −0.655 PtrHSF9 Potri.004G062300.1 A4a 407 Chr04 46 642.1 4.91 62.04 57.47 −0.843 PtrHSF10 Potri.005G214800.1 A7a 359 Chr05 40 692.4 5.37 61.42 66.48 −0.914 PtrHSF11 Potri.006G049200.1 B3 226 Chr06 26 377.0 9.06 76.77 51.80 −0.753 PtrHSF12 Potri.006G115700.1 A3 444 Chr06 49 881.0 4.86 66.94 61.80 −0.634 PtrHSF13 Potri.006G148200.1 A9 430 Chr06 48 496.8 5.40 73.23 51.38 −0.626 PtrHSF14 Potri.006G226800.1 A2 388 Chr06 43 856.9 4.70 73.30 56.80 −0.592 PtrHSF15 Potri.007G043800.1 B1 285 Chr07 31 018.9 4.57 59.58 37.61 −0.853 PtrHSF16 Potri.008G157600.1 A6b 348 Chr08 40 084.0 4.90 75.89 57.84 −0.692 PtrHSF17 Potri.009G068000.1 B4b 272 Chr09 31 530.7 7.19 72.68 57.32 −0.586 PtrHSF18 Potri.010G082000.1 A6a 358 Chr10 41 335.3 4.90 67.21 55.43 −0.788 PtrHSF19 Potri.010G104300.1 A8b 392 Chr10 44 690.9 4.42 70.61 43.14 −0.705 PtrHSF20 Potri.011G051600.1 A1 211 Chr11 24 383.6 9.79 63.84 53.41 −0.772 PtrHSF21 Potri.011G071700.1 A4a 406 Chr11 46 266.6 5.02 66.28 54.95 −0.793 PtrHSF22 Potri.012G138900.1 B2a 301 Chr12 33 366.2 4.77 67.94 50.83 −0.667 PtrHSF23 Potri.013G079800.1 A1b 499 Chr13 55 091.5 5.62 65.03 57.66 −0.619 PtrHSF24 Potri.014G027100.1 B4c 368 Chr14 41 038.2 8.17 68.10 52.12 −0.564 PtrHSF25 Potri.014G141400.1 A4b 443 Chr14 50 781.7 6.17 65.15 62.50 −0.806 PtrHSF26 Potri.015G141100.1 B2c 286 Chr15 31 751.8 4.86 80.66 50.80 −0.470 PtrHSF27 Potri.016G056500.1 B3b 228 Chr16 26 486.0 7.30 71.84 55.59 −0.732 PtrHSF28 Potri.017G059600.1 A5a 485 Chr17 54 386.4 5.84 69.01 57.90 −0.752 PtrHSF29 Potri.T137400.1 C1 339 Scaffold-294 37 981.9 5.27 77.05 51.81 −0.409
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表 3 杨树HSF家族基因启动子顺式作用元件
Table 3 Cis-acting elements of HSF family gene promoter in poplar
作用元件 Acting element 序列 Sequence 功能 Function Gap-box CAAATGAA(A/G)A 光响应元件的一部分 Part of light responsive element Box4 ATTAAT 与光相关的保守DNA模块的一部分 Part of a conserved DNA module involved in light DRE core GCCGAC 脱水反应元件 Dehydration responsive element MYC CATTTG 参与低温反应 Involved in chilling response MYB CAACCA MYB 结合位点 MYB binding site ARE AAACCA 无氧诱导所必需的 Essential for anaerobic induction ABRE ACGTG 参与脱落酸反应 Involved in abscisic acid responsiveness TGACG-motif TGACG 参与了MeJA反应 Involved in MeJA-responsiveness TC-rich repeats ATTCTCTAAC 参与防御和压力反应 Involved in defense and stress responsiveness TCA-element CCATCTTTTT 参与水杨酸反应 Involved in salicylic acid responsiveness LTR CCGAAA 参与低温反应 Involved in low-temperature responsiveness MBS CAACTG 参与干旱诱导 Involved in drought-inducibility MBS І aaaAaaC(G/C)GTTA 参与类黄酮生物合成基因调控 Involved in flavonoid biosynthetic gene regulation GARE-motif TCTGTTG 赤霉素反应元件 Gibberellins-responsive element AE-box AGAAACTT 光响应模块的一部分 Part of a module for light response WUN-motif AAATTACT 创伤反应元件 Wound-responsive element P-box CCTTTTG 赤霉素反应元件 Gibberellin-responsive element TGA-box 生长素反应元件的一部分 Part of an auxin-responsive element ERE ATTTTAAA 乙烯反应元件 Ethylene-responsive element G-box CACGTC/TACGTG 光响应性和结合其他特定压力调节的元件
Light responsiveness and combines with other regulatory elements under specific stress
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[1] Kerchev P, van der Meer T, Sujeeth N, et al. Molecular priming as an approach to induce tolerance against abiotic and oxidative stresses in crop plants[J]. Biotechnology Advances, 2020, 40: 107503. doi: 10.1016/j.biotechadv.2019.107503.
[2] Przemysław Ł K, Dominika R, Eva I, et al. Influence of abiotic stress factors on the antioxidant properties and polyphenols profile composition of green barley (Hordeum vulgare L.)[J]. International Journal of Molecular Sciences, 2020, 21(2): 397.
[3] Yang X H, Liang Z, Lu C. Genetic engineering of the biosynthesis of glycinebetaine enhances photosynthesis against high temperature stress in transgenic tobacco plants[J]. Plant Physiology, 2005, 138(4): 2299−2309. doi: 10.1104/pp.105.063164.
[4] Gao S, Han H, Feng H L, et al. Overexpression and suppression of violaxanthin de-epoxidase affects the sensitivity of photosystem II photoinhibition to high light and chilling stress in transgenic tobacco[J]. Journal of Integrative Plant Biology, 2010, 52(3): 332−339. doi: 10.1111/j.1744-7909.2010.00891.x.
[5] Lu Y. Identification and roles of photosystem II assembly, stability, and repair factors in Arabidopsis[J]. Frontiers in Plant Science, 2016, 7: 168.
[6] Murata N, Allakhverdiev S I, Nishiyama Y. The mechanism of photoinhibition in vivo: re-evaluation of the roles of catalase, a-tocopherol, non-photochemical quenching, and electron transport[J]. Biochimica et Biophysica Acta, 2012, 1817(8): 1127−1133. doi: 10.1016/j.bbabio.2012.02.020.
[7] Min L, Li Y Y, Hu Q, et al. Sugar and auxin signaling pathways respond to high-temperature stress during anther development as revealed by transcript profiling analysis in cotton[J]. Plant Physiology, 2014, 164(3): 1293−1308. doi: 10.1104/pp.113.232314.
[8] Hirt H, Shinozaki K. Plant responses to abiotic stress[M]. Berlin: Springer Heidelberg, 2004: 4.
[9] Huang Y C, Niu C Y, Yang C R, et al. The heat stress factor HSFA6b connects ABA signaling and ABA-mediated heat responses[J]. Plant Physiology, 2016, 172(2): 1182−1199.
[10] Nover N, Bharti K, Döing P, et al. Arabidopsis and the heat stress transcription factor world: how many heat stress transcription factors do we need?[J]. Cell Stress & Chaperones, 2001, 6(3): 177−189.
[11] Zhang J, Jia H X, Li J B, et al. Molecular evolution and expression divergence of the Populus euphratica Hsf genes provide insight into the stress acclimation of desert poplar[J]. Scientific Reports, 2016, 6: 30050. doi: 10.1038/srep30050
[12] Guo M, Liu J H, Ma X, et al. The plant heat stress transcription factors (HSFs): structure, regulation, and function in response to abiotic stresses[J]. Frontiers in Plant Science, 2016, 7: 114.
[13] Zupanska A K, LeFrois C, Ferl R J, et al. HSFA2
functions in the physiological adaptation of undifferentiated plant cells to spaceflight[J]. International Journal of Molecular Sciences, 2019, 20(2): 390. doi: 10.3390/ijms20020390. [14] Zang D, Wang J X, Zhang X, et al. Arabidopsis heat shock transcription factor HSFA7b positively mediates salt stress tolerance by binding to an E-box-like motif to regulate gene expression[J]. Journal of Experimental Botany, 2019, 70(19): 5355−5374. doi: 10.1093/jxb/erz261.
[15] 姚文静. 杨树转录因子ERF76基因耐盐功能研究[D]. 哈尔滨: 东北林业大学, 2016. Yao W J. Functional analysis of poplar transcription factor ERF76 gene on salt-stress tolerance[D]. Harbin: Northeast Forestry University, 2016.
[16] Tang M J, Xu L, Wang Y, et al. Genome-wide characterization and evolutionary analysis of heat shock transcription factors (HSFs) to reveal their potential role under abiotic stresses in radish (Raphanus sativus L.)[J]. BMC Genomics, 2019, 20(1): 1−13. doi: 10.1186/s12864-018-5379-1.
[17] Scharf K D, Berberich T, Ebersberger I, et al. The plant heat stress transcription factor (Hsf) family: structure, function and evolution[J]. Biochimica et Biophysica Acta (BBA): Gene Regulatory Mechanisms, 2012, 1819(2): 104−119. doi: 10.1016/j.bbagrm.2011.10.002.
[18] Peteranderl R, Rabenstein M, Shin Y K, et al. Biochemical and biophysical characterization of the trimerization domain from the heat shock transcription factor[J]. Biochemistry, 1999, 38(12): 3559−3569. doi: 10.1021/bi981774j.
[19] 李春艳. AP1基因转化双单倍体小黑杨及其数字基因表达谱分析[D]. 哈尔滨: 东北林业大学, 2013. Li C Y. Genetic transformation of AP1 gene in haploid Populus simonii × P. nigra and the DEGS analysis[D]. Harbin: Northeast Forestry University, 2013.
[20] 牛京萍, 刘轶, 由香玲. 小黑杨花粉植株的获得及遗传转化[J]. 福建林业科技, 2016, 43(4):13−16. Niu J P, Liu Y, You X L. Induction and genetic transformation of pollen haploid plants of Populus simonii × P. nigra[J]. Fujian Forestry Science and Technology, 2016, 43(4): 13−16.
[21] Deutsch F, Kumlehn J, Ziegenhagen B, et al. Stable haploid poplar callus lines from immature pollen culture[J]. Physiologia Plantarum, 2004, 120(4): 613−622.
[22] 彭儒胜, 赵大根, 张兴芬, 等. 杨树单倍体育种及其影响因素[J]. 防护林科技, 2007, 25(6):59−60, 73. doi: 10.3969/j.issn.1005-5215.2007.06.023. Peng R S, Zhao D G, Zhang X F, et al. Haploid breeding of poplar and its influencing factors[J]. Shelterbelt Technology, 2007, 25(6): 59−60, 73. doi: 10.3969/j.issn.1005-5215.2007.06.023.
[23] 王家玉, 赵威威. 银中杨、小黑杨树种的特性分析[J]. 科技风, 2011, 24(7):203. doi: 10.3969/j.issn.1671-7341.2011.07.179. Wang J Y, Zhao W W. Characteristics of Populus alba × P. berolinensis and Populus simonii × P. nigra[J]. Technology Wind, 2011, 24(7): 203. doi: 10.3969/j.issn.1671-7341.2011.07.179.
[24] von Koskull-Döring P, Scharf K D, Nover L. The diversity of plant heat stress transcription factors[J]. Trends in Plant Science, 2007, 12(10): 452−457. doi: 10.1016/j.tplants.2007.08.014.
[25] Liu B, Hu J J, Zhang J. Evolutionary divergence of duplicated Hsf genes in Populus[J]. Cells, 2019, 8(5): 438. doi: 10.3390/cells8050438.
[26] Akerfelt M, Morimoto R I, Sistonen L. Heat shock factors: integrators of cell stress, development and lifespan[J]. Nature Reviews Molecular Cell Biology, 2010, 11(8): 545−555. doi: 10.1038/nrm2938
[27] Fitter A H. Rapid changes in flowering time in British plants[J]. Science, 2002, 296: 1689−1691. doi: 10.1126/science.1071617.
[28] Alcazar R, Parker J E. The impact of temperature on balancing immune responsiveness and growth in Arabidopsis[J]. Trends Plant Sci, 2011, 16(12): 666−675. doi: 10.1016/j.tplants.2011.09.001.
[29] Gray S B, Brady S M. Plant developmental responses to climate change[J]. Developmental Biology, 2016, 419(1): 64−77. doi: 10.1016/j.ydbio.2016.07.023.
[30] Zha Q, Xi X J, He Y, et al. Transcriptomic analysis of the leaves of two grapevine cultivars under high-temperature stress[J]. Scientia Horticulturae, 2020, 265: 109265.
[31] 李思达. 小黑杨PxbHLH01/02基因在逆境胁迫中的功能分析[D]. 哈尔滨: 东北林业大学, 2018. Li S D. Functional analysis of PxbHLH01/02 genes in Populus simonii × P. nigra under stress condition[D]. Harbin: Northeast Forestry University, 2018.
[32] Charng Y Y, Liu H C, Liu N Y, et al. A heat-inducible transcription factor, HsfA2, is required for extension of acquired thermotolerance in Arabidopsis[J]. Plant Physiology, 2007, 143(1): 251−262. doi: 10.1104/pp.106.091322.
[33] Jung H S, Crisp P A, Estavillo G M, et al. Subset of heat-shock transcription factors required for the early response of Arabidopsis to excess light[J]. Proceedings of the National Academy of Sciences, 2013, 110(35): 14474−14479. doi: 10.1073/pnas.1311632110.
[34] 刘中原, 刘峥, 徐颖, 等. 白桦HSFA4转录因子的克隆及耐盐功能分析[J]. 林业科学, 2020, 56(5):69−79. Liu Z Y, Liu Z, Xu Y, et al. Cloning and salt tolerance analysis of transcription factor HSFA4 from Betula platyphylla[J]. Forestry Science, 2020, 56(5): 69−79.
[35] Perez-Salamo I, Papdi C, Rigo G, et al. The heat shock factor A4A confers salt tolerance and is regulated by oxidative stress and the mitogen-activated protein kinases MPK3 and MPK6[J]. Plant Physiology, 2014, 165(1): 319−334. doi: 10.1104/pp.114.237891.
[36] Chauhan H, Khurana N, Agarwal P, et al. A seed preferential heat shock transcription factor from wheat provides abiotic stress tolerance and yield enhancement in transgenic Arabidopsis under heat stress environment[J]. PLoS ONE, 2013, 8(11): e79577. doi: 10.1371/journal.pone.0079577.
[37] Bian X H, Li W, Niu C F, et al. A class B heat shock factor selected for during soybean domestication contributes to salt tolerance by promoting flavonoid biosynthesis[J]. New Phytologist, 2020, 225(1): 268−283. doi: 10.1111/nph.16104.
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