Wheat HD-Zip Gene Family： Identification and Response to Fusarium graminearum

doi:10.13560/j.cnki.biotech.bull.1985.2025-1109

Abstract

Abstract:

Objective To systematically identify the members of the wheat homeodomain-leucine zipper (HD-Zip) gene family, analyze their expression patterns across different tissues and developmental stages, and investigate their roles in response to Fusarium graminearum, thereby providing a theoretical basis for functional characterization of the wheat HD-Zip gene family. Method Using Arabidopsis HD-Zip protein sequences as queries, the members of the wheat HD-Zip gene family were identified from the wheat genome database. Protein physicochemical properties, phylogenetic tree construction, chromosome mapping and gene structure analysis were analyzed. Furthermore, transcriptome data and RT-qPCR were employed to assess the expression profiles of these genes in various tissues and under F. graminearum infection. Result A total of 85 wheat HD-Zip genes were identified, all of which encoded hydrophilic proteins, and were predicted to be unstable. Subcellular localization indicated that most HD-Zip proteins were localized in the nucleus and chloroplast. Phylogenetic and structural analyses revealed that these genes were grouped into four evolutionary clades, with members of the same clade showing high similarity in gene structure and conserved motifs, and were unevenly distributed across 22 chromosomes. Promoter analysis indicated the widespread presence of cis-acting elements associated with abscisic acid (ABA), gibberellin (GA), methyl jasmonate (MeJA), salicylic acid (SA), and auxin (IAA), as well as elements involved in stress responses, root specificity, and endosperm regulation. Expression analysis showed that 65 genes were expressed in the spikes, leaves, shoots, roots, and grains. Notably, under F. graminearum infection, genes such as TaHDZ1.1-6B, TaHDZ1.1-5A, TaHDZ1.1-5B, and TaHDZ1.1-5D were significantly upregulated at multiple time points, exhibiting consistent inducible expression patterns in both resistant and susceptible cultivars. Conclusion The wheat HD-Zip gene family presents strong evolutionary conservation and is likely involved in both organ development and responses to biotic and abiotic stresses through differential expression. Among them, TaHDZ1.1-6B, TaHDZ1.1-5A and TaHDZ1.1-5B may play crucial roles in wheat defense against F. graminearum.

Key words: wheat, HD-Zip gene family, expression analysis, stress response, Fusarium graminearum response

LYU Zheng, LIAN Ru-ying, LIU Yi-de, LIU Yi-ke, NING Qiang, WANG Shu-ping. Wheat HD-Zip Gene Family： Identification and Response to Fusarium graminearum[J]. Biotechnology Bulletin, 2026, 42(8): 123-132.

Figures/Tables 7

Fig. 1 Distribution of HD-Zip on chromosomes in wheat

Fig. 2 Phylogenetic tree of HD-Zip gene family in wheat and Arabidopsis

Fig. 3 Phylogenetic analysis, conserved structure and gene characterization of the wheat HD-Zip gene familyA: Phylogenetic relationships. B: Conserved motifs. C: Conservative domain. D: Gene structure

Fig. 4 Cis-acting elements in the wheat HD-Zip gene family

Fig. 5 Tissue-specific expression patterns of wheat HD-Zip gene family

Fig. 6 Expression patterns of wheat HD-Zip gene family under biotic and abiotic stress

Fig. 7 Expression patterns of HD-Zip gene under the inoculation of F. graminearum in wheat

References 42

[1]	汪宏凯, 王璇, 周雅琦, 等. 小麦赤霉病生物防治研究进展 [J]. 植物病理学报, 2025, 55(4): 818-831.
	Wang HK, Wang X, Zhou YQ, et al. Progresses in biological control of Fusarium head blight [J]. Acta Phytopathol Sin, 2025, 55(4): 818-831.
[2]	Elhiti M, Stasolla C. Structure and function of homodomain-leucine zipper (HD-Zip) proteins [J]. Plant Signal Behav, 2009, 4(2): 86-88.
[3]	Gao DL, Appiano M, Huibers RP, et al. Activation tagging of ATHB13 in Arabidopsis thaliana confers broad-spectrum disease resistance [J]. Plant Mol Biol, 2014, 86(6): 641-653.
[4]	Manavella PA, Dezar CA, Bonaventure G, et al. HAHB4, a sunflower HD-Zip protein, integrates signals from the jasmonic acid and ethylene pathways during wounding and biotic stress responses [J]. Plant J, 2008, 56(3): 376-388.
[5]	Sessa G, Carabelli M, Possenti M, et al. Multiple links between HD-Zip proteins and hormone networks [J]. Int J Mol Sci, 2018, 19(12): 4047.
[6]	Maré A, Boshoff WHP, Herselman L. Molecular breeding of wheat lines for multiple rust and Fusarium head blight resistance [J]. Euphytica, 2020, 216(10): 163.
[7]	Ariel FD, Manavella PA, Dezar CA, et al. The true story of the HD-Zip family [J]. Trends Plant Sci, 2007, 12(9): 419-426.
[8]	Wang YJ, Wang HJ, Yu C, et al. Comprehensive bioinformation analysis of homeodomain-leucine zipper gene family and expression pattern of HD-Zip I under abiotic stress in Salix suchowensis [J]. BMC Genomics, 2024, 25(1): 182.
[9]	Landschulz WH, Johnson PF, McKnight SL. The leucine zipper: a hypothetical structure common to a new class of DNA binding proteins [J]. Science, 1988, 240(4860): 1759-1764.
[10]	李俐, 王义, 王康宇, 等. HD-Zip基因家族的结构、功能与表达模式 [J]. 分子植物育种, 2018, 16(3): 781-790.
	Li L, Wang Y, Wang KY, et al. The structure, function and expression pattern of HD-Zip gene family [J]. Mol Plant Breed, 2018, 16(3): 781-790.
[11]	Agalou A, Purwantomo S, Overnäs E, et al. A genome-wide survey of HD-Zip genes in rice and analysis of drought-responsive family members [J]. Plant Mol Biol, 2008, 66(1/2): 87-103.
[12]	Qiu X, Wang GR, Abou-Elwafa SF, et al. Genome-wide identification of HD-ZIP transcription factors in maize and their regulatory roles in promoting drought tolerance [J]. Physiol Mol Biol Plants, 2022, 28(2): 425-437.
[13]	Li Y, Xiong HY, Cuo DJ, et al. Genome-wide characterization and expression profiling of the relation of the HD-Zip gene family to abiotic stress in barley (Hordeum vulgare L.) [J]. Plant Physiol Biochem, 2019, 141: 250-258.
[14]	Chen X, Chen Z, Zhao HL, et al. Genome-wide analysis of soybean HD-Zip gene family and expression profiling under salinity and drought treatments [J]. PLoS One, 2014, 9(2): e87156.
[15]	Sharif R, Raza A, Chen P, et al. HD-ZIP gene family: potential roles in improving plant growth and regulating stress-responsive mechanisms in plants [J]. Genes, 2021, 12(8): 1256.
[16]	刘娇, 帅鹏. HD-ZIP转录因子响应病菌与非生物胁迫研究进展 [J]. 福建农业学报, 2021, 36(1): 124-134.
	Liu J, Shuai P. Research progress on HD-ZIP transcription factors in response to pathogenic or abiotic stresses [J]. Fujian J Agric Sci, 2021, 36(1): 124-134.
[17]	Ponting CP, Aravind L. START: a lipid-binding domain in StAR, HD-ZIP and signalling proteins [J]. Trends Biochem Sci, 1999, 24(4): 130-132.
[18]	Mukherjee K, Bürglin TR. MEKHLA, a novel domain with similarity to PAS domains, is fused to plant homeodomain-leucine zipper Ⅲ proteins [J]. Plant Physiol, 2006, 140(4): 1142-1150.
[19]	Harris JC, Hrmova M, Lopato S, et al. Modulation of plant growth by HD-Zip class I and Ⅱ transcription factors in response to environmental stimuli [J]. New Phytol, 2011, 190(4): 823-837.
[20]	Ré DA, Capella M, Bonaventure G, et al. Arabidopsis AtHB7 and AtHB12 evolved divergently to fine tune processes associated with growth and responses to water stress [J]. BMC Plant Biol, 2014, 14: 150.
[21]	Jiao P, Jiang ZZ, Wei XT, et al. Overexpression of the homeobox-leucine zipper protein ATHB-6 improves the drought tolerance of maize (Zea mays L.) [J]. Plant Sci, 2022, 316: 111159.
[22]	Miguel VN, Manavella PA, Chan RL, et al. The AtHB1 transcription factor controls the miR164-CUC2 regulatory node to modulate leaf development [J]. Plant Cell Physiol, 2020, 61(3): 659-670.
[23]	Dezar CA, Giacomelli JI, Manavella PA, et al. HAHB10, a sunflower HD-Zip Ⅱ transcription factor, participates in the induction of flowering and in the control of phytohormone-mediated responses to biotic stress [J]. J Exp Bot, 2011, 62(3): 1061-1076.
[24]	Liu L, Zhang LC, Yang LH, et al. Genome-wide characterization and expression analysis of the HD-Zip Ⅱ gene family in response to drought and GA₃ stresses in Nicotiana tabacum [J]. Mol Biol Rep, 2024, 51(1): 581.
[25]	Li YX, Yang ZR, Zhang YY, et al. The roles of HD-ZIP proteins in plant abiotic stress tolerance [J]. Front Plant Sci, 2022, 13: 1027071.
[26]	Zhu TT, Wang L, Rimbert H, et al. Optical maps refine the bread wheat Triticum aestivum cv. Chinese Spring genome assembly [J]. Plant J, 2021, 107(1): 303-314.
[27]	Buerstmayr M, Steiner B, Buerstmayr H. Breeding for Fusarium head blight resistance in wheat-progress and challenges [J]. Plant Breed, 2020, 139(3): 429-454.
[28]	Sakr N, Al-Attar J. Screening for wheat resistance and pathogenicity of Fusarium head blight species using an in vitro detached head test [J]. Arch Phytopathol Plant Prot, 2021, 54(19/20): 2423-2439.
[29]	Zhu ZW, Chen L, Zhang W, et al. Genome-wide association analysis of Fusarium head blight resistance in Chinese elite wheat lines [J]. Front Plant Sci, 2020, 11: 206.
[30]	胡文静, 张春梅, 吴迪, 等. 长江中下游小麦抗赤霉病品种的筛选与部分农艺性状分析 [J]. 中国农业科学, 2020, 53(21): 4313-4321.
	Hu WJ, Zhang CM, Wu D, et al. Screening for resistance to Fusarium head blight and agronomic traits of wheat germplasms from Yangtze River Region [J]. Sci Agric Sin, 2020, 53(21): 4313-4321.
[31]	李雅倩, 王林, 宋婧含, 等. 小麦NPR1基因家族鉴定及其表达分析 [J]. 南方农业学报, 2021, 52(9): 2339-2349.
	Li YQ, Wang L, Song JH, et al. Genome-wide identification and expression analysis of wheat NPR1 gene family [J]. J South Agric, 2021, 52(9): 2339-2349.
[32]	葛仕杰, 刘怡德, 张华东, 等. 小麦蛋白质二硫键异构酶基因家族的鉴定与表达 [J]. 生物技术通报, 2025, 41(2): 85-96.
	Ge SJ, Liu YD, Zhang HD, et al. Identification and expression analysis of protein disulfide isomerase gene family in wheat [J]. Biotechnol Bull, 2025, 41(2): 85-96.
[33]	Pan G, Li Z, Yin M, et al. Genome-wide identification, expression, and sequence analysis of CONSTANS-like gene family in Cannabis reveals a potential role in plant flowering time regulation [J]. BMC Plant Biol, 2021, 21(1): 142.
[34]	Hyeon Jeong J, Joo Jung W, Weon Seo Y. Genome-wide identification and expression analysis of the annexin gene family in rye (Secale cereale L.) [J]. Gene, 2022, 838: 146704.
[35]	Wen YY, Zhao ZY, Cheng LN, et al. Genome-wide identification and expression profiling of the ABI5 gene family in foxtail millet (Setaria italica) [J]. BMC Plant Biol, 2024, 24(1): 164.
[36]	Buerstmayr M, Wagner C, Nosenko T, et al. Fusarium head blight resistance in European winter wheat: insights from genome-wide transcriptome analysis [J]. BMC Genomics, 2021, 22(1): 470.
[37]	Sowa S, Sozoniuk M, Toporowska J, et al. Validation of reference genes as an internal control for studying Avena sativa-Puccinia coronata interaction by RT-qPCR [J]. Sci Rep, 2022, 12(1): 14601.
[38]	Dynan WS, Tjian R. Control of eukaryotic messenger RNA synthesis by sequence-specific DNA-binding proteins [J]. Nature, 1985, 316(6031): 774-778.
[39]	Yamaguchi-Shinozaki K, Shinozaki K. Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters [J]. Trends Plant Sci, 2005, 10(2): 88-94.
[40]	Hou SJ, Tsuda K. Salicylic acid and jasmonic acid crosstalk in plant immunity [J]. Essays Biochem, 2022, 66(5): 647-656.
[41]	Zhao Y, Ma Q, Jin XL, et al. A novel maize homeodomain-leucine zipper (HD-Zip) I gene, Zmhdz10, positively regulates drought and salt tolerance in both rice and Arabidopsis [J]. Plant Cell Physiol, 2014, 55(6): 1142-1156.
[42]	He YL, Fu XQ, Li L, et al. AaSPL9 affects glandular trichomes initiation by positively regulating expression of AaHD1 in Artemisia annua L. [J]. Plant Sci, 2022, 317: 111172.