[en] This review provides a detailed description of the function and mechanism of VQ family gene, which is helpful for further research and application of VQ gene resources to improve crops. Valine-glutamine (VQ) motif-containing proteins are a large class of transcriptional regulatory cofactors. VQ proteins have their own unique molecular characteristics. Amino acids are highly conserved only in the VQ domain, while other positions vary greatly. Most VQ genes do not contain introns and the length of their proteins is less than 300 amino acids. A majority of VQ proteins are predicted to be localized in the nucleus. The promoter of many VQ genes contains stress or growth related elements. Segment duplication and tandem duplication are the main amplification mechanisms of the VQ gene family in angiosperms and gymnosperms, respectively. Purification selection plays a crucial role in the evolution of many VQ genes. By interacting with WRKY, MAPK, and other proteins, VQ proteins participate in the multiple signaling pathways to regulate plant growth and development, as well as defense responses to biotic and abiotic stresses. Although there have been some reports on the VQ gene family in plants, most of them only identify family members, with little functional verification, and there is also a lack of complete, detailed, and up-to-date review of research progress. Here, we comprehensively summarized the research progress of VQ genes that have been published so far, mainly including their molecular characteristics, biological functions, importance of VQ motif, and working mechanisms. Finally, the regulatory network and model of VQ genes were drawn, a precise molecular breeding strategy based on VQ genes was proposed, and the current problems and future prospects were pointed out, providing a powerful reference for further research and utilization of VQ genes in plant improvement.
Disciplines :
Agriculture & agronomy
Author, co-author :
Tian, Jinfu ; Université de Liège - ULiège > Gembloux Agro-Bio Tech > Gembloux Agro-Bio Tech ; Institute of Crop Sciences, Chinese Academy of Agricultural Sciences (CAAS), Beijing, 100081, China
Zhang, Jiahui ; Institute of Crop Sciences, Chinese Academy of Agricultural Sciences (CAAS), Beijing, 100081, China ; Université de Liège - ULiège > Gembloux Agro-Bio Tech > Gembloux Agro-Bio Tech
Ahmad N, Jiang Z, Zhang L, Hussain I, Yang X (2023) Insights on phytohormonal crosstalk in plant response to nitrogen stress: a focus on plant root growth and development. Int J Mol Sci 24(4):3631. 10.3390/ijms24043631 DOI: 10.3390/ijms24043631
Ali MRM, Uemura T, Ramadan A, Adachi K, Nemoto K, Nozawa A et al (2019) The ring-type E3 ubiquitin ligase JUL1 targets the VQ-motif protein JAV1 to coordinate jasmonate signaling. Plant Physiol 179(4):1273–1284. 10.1104/pp.18.00715 DOI: 10.1104/pp.18.00715
Andreasson E, Jenkins T, Brodersen P, Thorgrimsen S, Petersen NH, Zhu S et al (2005) The MAP kinase substrate MKS1 is a regulator of plant defense responses. EMBO J 24(14):2579–2589. 10.1038/sj.emboj.7600737 DOI: 10.1038/sj.emboj.7600737
Baek M, DiMaio F, Anishchenko I, Dauparas J, Ovchinnikov S, Lee GR et al (2021) Accurate prediction of protein structures and interactions using a three-track neural network. Science 373(6557):871–876. 10.1126/science.abj8754 DOI: 10.1126/science.abj8754
Bailey TL, Johnson J, Grant CE, Noble WS (2015) The MEME suite. Nucleic Acids Res 43(W1):W39–W49. 10.1093/nar/gkv416 DOI: 10.1093/nar/gkv416
Bakshi M, Oelmüller R (2014) WRKY transcription factors: jack of many trades in plants. Plant Signal Behav 9(2):e27700. 10.4161/psb.27700 DOI: 10.4161/psb.27700
Ban Z, Estelle M (2021) CUL3 E3 ligases in plant development and environmental response. Nat Plants 7(1):6–16. 10.1038/s41477-020-00833-6 DOI: 10.1038/s41477-020-00833-6
Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69(4):473–488. 10.1007/s11103-008-9435-0 DOI: 10.1007/s11103-008-9435-0
Bi G, Zhou Z, Wang W, Li L, Rao S, Wu Y et al (2018) Receptor-like cytoplasmic kinases directly link diverse pattern recognition receptors to the activation of mitogen-activated protein kinase cascades in Arabidopsis. Plant Cell 30(7):1543–1561. 10.1105/tpc.17.00981 DOI: 10.1105/tpc.17.00981
Bigeard J, Hirt H (2018) Nuclear signaling of plant MAPKs. Front Plant Sci 9:469. 10.3389/fpls.2018.00469 DOI: 10.3389/fpls.2018.00469
Bryant P, Pozzati G, Elofsson A (2022) Improved prediction of protein-protein interactions using AlphaFold2. Nat Commun 13(1):1265. 10.1038/s41467-022-28865-w DOI: 10.1038/s41467-022-28865-w
Buscaill P, Rivas S (2014) Transcriptional control of plant defence responses. Curr Opin Plant Biol 20:35–46. 10.1016/j.pbi.2014.04.004 DOI: 10.1016/j.pbi.2014.04.004
Caarls L, Elberse J, Awwanah M, Ludwig NR, de Vries M, Zeilmaker T et al (2017) Arabidopsis JASMONATE-INDUCED OXYGENASES down-regulate plant immunity by hydroxylation and inactivation of the hormone jasmonic acid. Proc Natl Acad Sci USA 114(24):6388–6393. 10.1073/pnas.1701101114 DOI: 10.1073/pnas.1701101114
Cai H, Zhang M, Liu Y, He Q, Chai M, Liu L et al (2019) Genome-wide classification and evolutionary and functional analyses of the VQ family. Tropical Plant Biol 12:117–131. 10.1007/s12042-019-09224-4 DOI: 10.1007/s12042-019-09224-4
Cao Y, Meng D, Abdullah M, Jin Q, Lin Y, Cai Y (2018) Genome wide identification, evolutionary, and expression analysis of VQ genes from two Pyrus species. Genes 9(4):224. 10.3390/genes9040224 DOI: 10.3390/genes9040224
Chen J, Wang H, Li Y, Pan J, Hu Y, Yu D (2018) Arabidopsis VQ10 interacts with WRKY8 to modulate basal defense against Botrytis cinerea. J Integr Plant Biol 60(10):956–969. 10.1111/jipb.12664 DOI: 10.1111/jipb.12664
Chen P, Wei F, Cheng S, Ma L, Wang H, Zhang M et al (2020) A comprehensive analysis of cotton VQ gene superfamily reveals their potential and extensive roles in regulating cotton abiotic stress. BMC Genomics 21(1):795. 10.1186/s12864-020-07171-z DOI: 10.1186/s12864-020-07171-z
Chen S, Cao H, Huang B, Zheng X, Liang K, Wang GL et al (2022a) The WRKY10-VQ8 module safely and effectively regulates rice thermotolerance. Plant Cell Environ 45(7):2126–2144. 10.1111/pce.14329 DOI: 10.1111/pce.14329
Chen L, Wu L, Yang L, Yu H, Huang P, Wang Y et al (2022b) TcJAV3-TcWRKY26 cascade is a missing link in the jasmonate-activated expression of taxol biosynthesis gene DBAT in Taxus chinensis. Int J Mol Sci 23(21):13194. 10.3390/ijms232113194 DOI: 10.3390/ijms232113194
Cheng Y, Zhou Y, Yang Y, Chi YJ, Zhou J, Chen JY et al (2012) Structural and functional analysis of VQ motif-containing proteins in Arabidopsis as interacting proteins of WRKY transcription factors. Plant Physiol 159(2):810–825. 10.1104/pp.112.196816 DOI: 10.1104/pp.112.196816
Cheng X, Wang Y, Xiong R, Gao Y, Yan H, Xiang Y (2020) A Moso bamboo gene VQ28 confers salt tolerance to transgenic Arabidopsis plants. Planta 251(5):99. 10.1007/s00425-020-03391-5 DOI: 10.1007/s00425-020-03391-5
Cheng X, Gao C, Liu X, Xu D, Pan X, Gao W et al (2022a) Characterization of the wheat VQ protein family and expression of candidate genes associated with seed dormancy and germination. BMC Plant Biol 22(1):119. 10.1186/s12870-022-03430-1 DOI: 10.1186/s12870-022-03430-1
Cheng X, Yao H, Cheng Z, Tian B, Gao C, Gao W et al (2022b) The wheat gene TaVQ14 confers salt and drought tolerance in transgenic Arabidopsis thaliana plants. Front Plant Sci 13:870586. 10.3389/fpls.2022.870586 DOI: 10.3389/fpls.2022.870586
Chi Y, Yang Y, Zhou Y, Zhou J, Fan B, Yu JQ et al (2013) Protein-protein interactions in the regulation of WRKY transcription factors. Mol Plant 6(2):287–300. 10.1093/mp/sst026 DOI: 10.1093/mp/sst026
Chu W, Liu B, Wang Y, Pan F, Chen Z, Yan H et al (2016) Genome-wide analysis of poplar VQ gene family and expression profiling under PEG, NaCl, and SA treatments. Tree Genet Genomes 12:124. 10.1007/s11295-016-1082-z DOI: 10.1007/s11295-016-1082-z
Claeys H, Neyrinck E, Dumoulin L, Pharazyn A, Verstichele A, Pauwels L et al (2023) Coordinated gene upregulation in maize through CRISPR/Cas-mediated enhancer insertion. Plant Biotechnol J. 10.1111/pbi.14191 DOI: 10.1111/pbi.14191
Coll NS, Epple P, Dangl JL (2011) Programmed cell death in the plant immune system. Cell Death Differ 18(8):1247–1256. 10.1038/cdd.2011.37 DOI: 10.1038/cdd.2011.37
Considine MJ, Foyer CH (2021) Oxygen and reactive oxygen species-dependent regulation of plant growth and development. Plant Physiol 186(1):79–92. 10.1093/plphys/kiaa077 DOI: 10.1093/plphys/kiaa077
Dauparas J, Anishchenko I, Bennett N, Bai H, Ragotte RJ, Milles LF et al (2022) Robust deep learning-based protein sequence design using ProteinMPNN. Science 378(6615):49–56. 10.1126/science.add2187 DOI: 10.1126/science.add2187
Ding H, Yuan G, Mo S, Qian Y, Wu Y, Chen Q et al (2019) Genome-wide analysis of the plant-specific VQ motif-containing proteins in tomato (Solanum lycopersicum) and characterization of SlVQ6 in thermotolerance. Plant Physiol Biochem 143:29–39. 10.1016/j.plaphy.2019.08.019 DOI: 10.1016/j.plaphy.2019.08.019
Dong Q, Zhao S, Duan D, Tian Y, Wang Y, Mao K et al (2018) Structural and functional analyses of genes encoding VQ proteins in apple. Plant Sci 272:208–219. 10.1016/j.plantsci.2018.04.029 DOI: 10.1016/j.plantsci.2018.04.029
Dong Q, Duan D, Zheng W, Huang D, Wang Q, Li X et al (2021) MdVQ37 overexpression reduces basal thermotolerance in transgenic apple by affecting transcription factor activity and salicylic acid homeostasis. Hortic Res 8(1):220. 10.1038/s41438-021-00655-3 DOI: 10.1038/s41438-021-00655-3
Fiil BK, Petersen M (2011) Constitutive expression of MKS1 confers susceptibility to Botrytis cinerea infection independent of PAD3 expression. Plant Signal Behav 6(10):1425–1427. 10.4161/psb.6.10.16759 DOI: 10.4161/psb.6.10.16759
Gao C (2021) Genome engineering for crop improvement and future agriculture. Cell 184(6):1621–1635. 10.1016/j.cell.2021.01.005 DOI: 10.1016/j.cell.2021.01.005
Gargul JM, Mibus H, Serek M (2015) Manipulation of MKS1 gene expression affects Kalanchoë blossfeldiana and Petunia hybrida phenotypes. Plant Biotechnol J 13(1):51–61. 10.1111/pbi.12234 DOI: 10.1111/pbi.12234
Garrido-Gala J, Higuera JJ, Muñoz-Blanco J, Amil-Ruiz F, Caballero JL (2019) The VQ motif-containing proteins in the diploid and octoploid strawberry. Sci Rep 9(1):4942. 10.1038/s41598-019-41210-4 DOI: 10.1038/s41598-019-41210-4
Gayubas B, Castillo MC, Ramos S, León J (2023) Enhanced meristem development, tolerance to oxidative stress and hyposensitivity to nitric oxide in the hypermorphic vq10-H mutant in AtVQ10 gene. Plant Cell Environ 46:3445–3463. 10.1111/pce.14685 DOI: 10.1111/pce.14685
Goyal P, Devi R, Verma B, Hussain S, Arora P, Tabassum R et al (2023) WRKY transcription factors: evolution, regulation, and functional diversity in plants. Protoplasma 260(2):331–348. 10.1007/s00709-022-01794-7 DOI: 10.1007/s00709-022-01794-7
Guan Y, Meng X, Khanna R, LaMontagne E, Liu Y, Zhang S (2014) Phosphorylation of a WRKY transcription factor by MAPKs is required for pollen development and function in Arabidopsis. PLoS Genet 10(5):e1004384. 10.1371/journal.pgen.1004384 DOI: 10.1371/journal.pgen.1004384
Guo J, Chen J, Yang J, Yu Y, Yang Y, Wang W (2018) Identification, characterization and expression analysis of the VQ motif-containing gene family in tea plant (Camellia sinensis). BMC Genomics 19(1):710. 10.1186/s12864-018-5107-x DOI: 10.1186/s12864-018-5107-x
Halim VA, Vess A, Scheel D, Rosahl S (2006) The role of salicylic acid and jasmonic acid in pathogen defence. Plant Biol (Stuttg) 8(3):307–313. 10.1055/s-2006-924025 DOI: 10.1055/s-2006-924025
Hao Z, Tian J, Fang H, Fang L, Xu X, He F et al (2022) A VQ-motif-containing protein fine-tunes rice immunity and growth by a hierarchical regulatory mechanism. Cell Rep 40(7):111235. 10.1016/j.celrep.2022.111235 DOI: 10.1016/j.celrep.2022.111235
He Q, He M, Zhang X, Zhang X, Zhang W, Dong J et al (2023) RsVQ4-RsWRKY26 module positively regulates thermotolerance by activating RsHSP70–20 transcription in radish (Raphanus sativus L.). Environ Exp Bot 214:105467. 10.1016/j.envexpbot.2023.105467 DOI: 10.1016/j.envexpbot.2023.105467
Hu P, Zhou W, Cheng Z, Fan M, Wang L, Xie D (2013a) JAV1 controls jasmonate-regulated plant defense. Mol Cell 50(4):504–515. 10.1016/j.molcel.2013.04.027 DOI: 10.1016/j.molcel.2013.04.027
Hu Y, Chen L, Wang H, Zhang L, Wang F, Yu D (2013b) Arabidopsis transcription factor WRKY8 functions antagonistically with its interacting partner VQ9 to modulate salinity stress tolerance. Plant J 74(5):730–745. 10.1111/tpj.12159 DOI: 10.1111/tpj.12159
Hu L, Ye M, Li R, Zhang T, Zhou G, Wang Q et al (2015) The rice transcription factor WRKY53 suppresses herbivore-induced defenses by acting as a negative feedback modulator of mitogen-activated protein kinase activity. Plant Physiol 169(4):2907–2921. 10.1104/pp.15.01090 DOI: 10.1104/pp.15.01090
Huang H, Zhao W, Li C, Qiao H, Song S, Yang R et al (2022a) SlVQ15 interacts with jasmonate-ZIM domain proteins and SlWRKY31 to regulate defense response in tomato. Plant Physiol 190(1):828–842. 10.1093/plphys/kiac275 DOI: 10.1093/plphys/kiac275
Huang X, Huang S, Han B, Li J (2022b) The integrated genomics of crop domestication and breeding. Cell 185(15):2828–2839. 10.1016/j.cell.2022.04.036 DOI: 10.1016/j.cell.2022.04.036
Huang J, Lin Q, Fei H, He Z, Xu H, Li Y et al (2023) Discovery of deaminase functions by structure-based protein clustering. Cell 186(15):3182-3195.e14. 10.1016/j.cell.2023.05.041 DOI: 10.1016/j.cell.2023.05.041
Jiang Y, Deyholos MK (2009) Functional characterization of Arabidopsis NaCl-inducible WRKY25 and WRKY33 transcription factors in abiotic stresses. Plant Mol Biol 69(1–2):91–105. 10.1007/s11103-008-9408-3 DOI: 10.1007/s11103-008-9408-3
Jiang Y, Yu D (2016) The WRKY57 transcription factor affects the expression of jasmonate ZIM-domain genes transcriptionally to compromise Botrytis cinerea resistance. Plant Physiol 171(4):2771–2782. 10.1104/pp.16.00747 DOI: 10.1104/pp.16.00747
Jiang J, Ma S, Ye N, Jiang M, Cao J, Zhang J (2017) WRKY transcription factors in plant responses to stresses. J Integr Plant Biol 59(2):86–101. 10.1111/jipb.12513 DOI: 10.1111/jipb.12513
Jiang SY, Sevugan M, Ramachandran S (2018) Valine-glutamine (VQ) motif coding genes are ancient and non-plant-specific with comprehensive expression regulation by various biotic and abiotic stresses. BMC Genomics 19(1):342. 10.1186/s12864-018-4733-7 DOI: 10.1186/s12864-018-4733-7
Jing Y, Lin R (2015) The VQ motif-containing protein family of plant-specific transcriptional regulators. Plant Physiol 169(1):371–378. 10.1104/pp.15.00788 DOI: 10.1104/pp.15.00788
Jones JD, Dangl JL (2006) The plant immune system. Nature 444(7117):323–329. 10.1038/nature05286 DOI: 10.1038/nature05286
Ke Y, Deng H, Wang S (2017) Advances in understanding broad-spectrum resistance to pathogens in rice. Plant J 90(4):738–748. 10.1111/tpj.13438 DOI: 10.1111/tpj.13438
Khoso MA, Hussain A, Ritonga FN, Ali Q, Channa MM, Alshegaihi RM et al (2022) WRKY transcription factors (TFs): molecular switches to regulate drought, temperature, and salinity stresses in plants. Front Plant Sci 13:1039329. 10.3389/fpls.2022.1039329 DOI: 10.3389/fpls.2022.1039329
Kim DY, Kwon SI, Choi C, Lee H, Ahn I, Park SR et al (2013) Expression analysis of rice VQ genes in response to biotic and abiotic stresses. Gene 529(2):208–214. 10.1016/j.gene.2013.08.023 DOI: 10.1016/j.gene.2013.08.023
Kopriva S, Malagoli M, Takahashi H (2019) Sulfur nutrition: impacts on plant development, metabolism, and stress responses. J Exp Bot 70(16):4069–4073. 10.1093/jxb/erz319 DOI: 10.1093/jxb/erz319
Kumari A, Kaladhar VC, Yadav N, Singh P, Reddy K, Gupta KJ (2023) Nitric oxide regulates mitochondrial biogenesis in plants. Plant Cell Environ 46(8):2492–2506. 10.1111/pce.14637 DOI: 10.1111/pce.14637
Lai Z, Mengiste T (2013) Genetic and cellular mechanisms regulating plant responses to necrotrophic pathogens. Curr Opin Plant Biol 16(4):505–512. 10.1016/j.pbi.2013.06.014 DOI: 10.1016/j.pbi.2013.06.014
Lai Z, Li Y, Wang F, Cheng Y, Fan B, Yu JQ et al (2011) Arabidopsis sigma factor binding proteins are activators of the WRKY33 transcription factor in plant defense. Plant Cell 23(10):3824–3841. 10.1105/tpc.111.090571 DOI: 10.1105/tpc.111.090571
Lai X, Stigliani A, Vachon G, Carles C, Smaczniak C, Zubieta C et al (2019) Building transcription factor binding site models to understand gene regulation in plants. Mol Plant 12(6):743–763. 10.1016/j.molp.2018.10.010 DOI: 10.1016/j.molp.2018.10.010
Lan X, Wang X, Tao Q, Zhang H, Li J, Meng Y et al (2022) activation of the VQ motif-containing protein gene VQ28 compromised nonhost resistance of Arabidopsis thaliana to Phytophthora pathogens. Plants 11(7):858. 10.3390/plants11070858 DOI: 10.3390/plants11070858
Lei R, Li X, Ma Z, Lv Y, Hu Y, Yu D (2017) Arabidopsis WRKY2 and WRKY34 transcription factors interact with VQ20 protein to modulate pollen development and function. Plant J 91(6):962–976. 10.1111/tpj.13619 DOI: 10.1111/tpj.13619
Lei R, Ma Z, Yu D (2018) WRKY2/34-VQ20 modules in Arabidopsis thaliana negatively regulate expression of a trio of related MYB transcription factors during pollen development. Front Plant Sci 9:331. 10.3389/fpls.2018.00331 DOI: 10.3389/fpls.2018.00331
León J, Gayubas B, Castillo MC (2021) Valine-glutamine proteins in plant responses to oxygen and nitric oxide. Front Plant Sci 11:632678. 10.3389/fpls.2020.632678 DOI: 10.3389/fpls.2020.632678
Li S, Fu Q, Chen L, Huang W, Yu D (2011) Arabidopsis thaliana WRKY25, WRKY26, and WRKY33 coordinate induction of plant thermotolerance. Planta 233(6):1237–1252. 10.1007/s00425-011-1375-2 DOI: 10.1007/s00425-011-1375-2
Li Y, Jing Y, Li J, Xu G, Lin R (2014a) Arabidopsis VQ MOTIF-CONTAINING PROTEIN29 represses seedling deetiolation by interacting with PHYTOCHROME-INTERACTING FACTOR1. Plant Physiol 164(4):2068–2080. 10.1104/pp.113.234492 DOI: 10.1104/pp.113.234492
Li N, Li X, Xiao J, Wang S (2014b) Comprehensive analysis of VQ motif-containing gene expression in rice defense responses to three pathogens. Plant Cell Rep 33(9):1493–1505. 10.1007/s00299-014-1633-4 DOI: 10.1007/s00299-014-1633-4
Li X, Qin R, Du Q, Cai L, Hu D, Du H et al (2020a) Knockdown of GmVQ58 encoding a VQ motif-containing protein enhances soybean resistance to the common cutworm (Spodoptera litura Fabricius). J Exp Bot 71(10):3198–3210. 10.1093/jxb/eraa095 DOI: 10.1093/jxb/eraa095
Li W, Pang S, Lu Z, Jin B (2020b) Function and mechanism of WRKY transcription factors in abiotic stress responses of plants. Plants 9(11):1515. 10.3390/plants9111515 DOI: 10.3390/plants9111515
Li N, Yang Z, Li J, Xie W, Qin X, Kang Y et al (2021) Two VQ proteins are substrates of the OsMPKK6-OsMPK4 cascade in rice defense against bacterial blight. Rice (N.Y.) 14(1):39. 10.1186/s12284-021-00483-y DOI: 10.1186/s12284-021-00483-y
Li S, Luo Y, Wei G, Zong W, Zeng W, Xiao D (2023) Improving yield-related traits by editing the promoter of the heading date gene Ehd1 in rice. Theor Appl Genet 136(12):239. 10.1007/s00122-023-04489-6 DOI: 10.1007/s00122-023-04489-6
Ling L, Qu Y, Zhu J, Wang D, Guo C (2020) Genome-wide identification and expression analysis of the VQ gene family in Cicer arietinum and Medicago truncatula. PeerJ 8:e8471. 10.7717/peerj.8471 DOI: 10.7717/peerj.8471
Liu S, Hua L, Dong S, Chen H, Zhu X, Jiang J et al (2015) OsMAPK6, a mitogen-activated protein kinase, influences rice grain size and biomass production. Plant J 84(4):672–681. 10.1111/tpj.13025 DOI: 10.1111/tpj.13025
Liu C, Liu H, Zhou C, Timko MP (2020) Genome-Wide Identification of the VQ protein gene family of tobacco (Nicotiana tabacum L.) and analysis of its expression in response to phytohormones and abiotic and biotic stresses. Genes 11(3):284. 10.3390/genes11030284 DOI: 10.3390/genes11030284
Liu Y, Liu X, Yang D, Yin Z, Jiang Y, Ling H et al (2022a) A comprehensive identification and expression analysis of VQ motif-containing proteins in sugarcane (Saccharum spontaneum L.) under phytohormone treatment and cold stress. Int J Mol Sci 23(11):6334. 10.3390/ijms23116334 DOI: 10.3390/ijms23116334
Liu S, Wang Z, Wu J, Wu C, Xiong R, Xiang Y et al (2022b) The poplar VQ1 gene confers salt tolerance and pathogen resistance in transgenic Arabidopsis plants via changes in hormonal signaling. G3 12(4):044. 10.1093/g3journal/jkac044 DOI: 10.1093/g3journal/jkac044
Liu M, Li C, Li Y, An Y, Ruan X, Guo Y et al (2023) Genome-wide identification and characterization of the VQ motif-containing gene family based on their evolution and expression analysis under abiotic stress and hormone treatments in foxtail millet (Setaria italic L.). Genes 14(5):1032–8. 10.3390/genes14051032 DOI: 10.3390/genes14051032
Luo M, Dennis ES, Berger F, Peacock WJ, Chaudhury A (2005) MINISEED3 (MINI3), a WRKY family gene, and HAIKU2 (IKU2), a leucine-rich repeat (LRR) KINASE gene, are regulators of seed size in Arabidopsis. Proc Natl Acad Sci USA 102(48):17531–17536. 10.1073/pnas.0508418102 DOI: 10.1073/pnas.0508418102
Lutz ID, Wang S, Norn C, Courbet A, Borst AJ, Zhao YT et al (2023) Top-down design of protein architectures with reinforcement learning. Science 380(6642):266–273. 10.1126/science.adf6591 DOI: 10.1126/science.adf6591
Ma H, Chen J, Zhang Z, Ma L, Yang Z, Zhang Q et al (2017) MAPK kinase 10.2 promotes disease resistance and drought tolerance by activating different MAPKs in rice. Plant J 92(4):557–570. 10.1111/tpj.13674 DOI: 10.1111/tpj.13674
Ma J, Ling L, Huang X, Wang W, Wang Y, Zhang M et al (2021) Genome-wide identification and expression analysis of the VQ gene family in sunflower (Helianthus annuus L.). J Plant Biochem Biotechnol 30:56–66. 10.1007/s13562-020-00568-7 DOI: 10.1007/s13562-020-00568-7
Ma J, Li C, Sun L, Ma X, Qiao H, Zhao W et al (2023a) The SlWRKY57-SlVQ21/SlVQ16 module regulates salt stress in tomato. J Integr Plant Biol 65(11): 2437–2455. 10.1111/jipb.13562 DOI: 10.1111/jipb.13562
Ma J, Wang R, Zhao H, Li L, Zeng F, Wang Y et al (2023b) Genome-wide characterization of the VQ genes in Triticeae and their functionalization driven by polyploidization and gene duplication events in wheat. Int J Biol Macromol 243:125264. 10.1016/j.ijbiomac.2023.125264 DOI: 10.1016/j.ijbiomac.2023.125264
Madani A, Krause B, Greene ER, Subramanian S, Mohr BP, Holton JM et al (2023) Large language models generate functional protein sequences across diverse families. Nat Biotechnol 41(8):1099–1106. 10.1038/s41587-022-01618-2 DOI: 10.1038/s41587-022-01618-2
Meldau S, Ullman-Zeunert L, Govind G, Bartram S, Baldwin IT (2012) MAPK-dependent JA and SA signalling in Nicotiana attenuata affects plant growth and fitness during competition with conspecifics. BMC Plant Biol 12:213. 10.1186/1471-2229-12-213 DOI: 10.1186/1471-2229-12-213
Meng X, Zhang S (2013) MAPK cascades in plant disease resistance signaling. Annu Rev Phytopathol 51:245–266. 10.1146/annurev-phyto-082712-102314 DOI: 10.1146/annurev-phyto-082712-102314
Meng X, Lu M, Xia Z, Li H, Liu D, Li K et al (2023) Wheat VQ motif-containing protein VQ25-A facilitates leaf senescence via the abscisic acid pathway. Int J Mol Sci 24:13839. 10.3390/ijms241813839 DOI: 10.3390/ijms241813839
Miller RN, Costa Alves GS, Van Sluys MA (2017) Plant immunity: unravelling the complexity of plant responses to biotic stresses. Ann Bot 119(5):681–687. 10.1093/aob/mcw284 DOI: 10.1093/aob/mcw284
Molla KA, Sretenovic S, Bansal KC, Qi Y (2021) Precise plant genome editing using base editors and prime editors. Nat Plants 7(9):1166–1187. 10.1038/s41477-021-00991-1 DOI: 10.1038/s41477-021-00991-1
Morikawa K, Shiina T, Murakami S, Toyoshima Y (2002) Novel nuclear-encoded proteins interacting with a plastid sigma factor, Sig1, Arabidopsis thaliana. FEBS Lett 514(2–3):300–304. 10.1016/s0014-5793(02)02388-8 DOI: 10.1016/s0014-5793(02)02388-8
Myers RJ, Fichman Y, Zandalinas SI, Mittler R (2023) Jasmonic acid and salicylic acid modulate systemic reactive oxygen species signaling during stress responses. Plant Physiol 191(2):862–873. 10.1093/plphys/kiac449 DOI: 10.1093/plphys/kiac449
Narusaka M, Kawai K, Izawa N, Seki M, Shinozaki K, Seo S et al (2008) Gene coding for SigA-binding protein from Arabidopsis appears to be transcriptionally up-regulated by salicylic acid and NPR1-dependent mechanisms. J Gen Plant Pathol 74:345–354. 10.1007/s10327-008-0117-1 DOI: 10.1007/s10327-008-0117-1
Ninkuu V, Yan J, Fu Z, Yang T, Ziemah J, Ullrich MS et al (2022) Lignin and its pathway-associated phytoalexins modulate plant defense against fungi. J Fungi 9(1):52. 10.3390/jof9010052 DOI: 10.3390/jof9010052
Oliva M, Farcot E, Vernoux T (2013) Plant hormone signaling during development: insights from computational models. Curr Opin Plant Biol 16(1):19–24. 10.1016/j.pbi.2012.11.006 DOI: 10.1016/j.pbi.2012.11.006
Pan J, Wang H, Hu Y, Yu D (2018) Arabidopsis VQ18 and VQ26 proteins interact with ABI5 transcription factor to negatively modulate ABA response during seed germination. Plant J 95(3):529–544. 10.1111/tpj.13969 DOI: 10.1111/tpj.13969
Parisi K, Shafee TMA, Quimbar P, van der Weerden NL, Bleackley MR, Anderson MA (2019) The evolution, function and mechanisms of action for plant defensins. Semin Cell Dev Biol 88:107–118. 10.1016/j.semcdb.2018.02.004 DOI: 10.1016/j.semcdb.2018.02.004
Pauwels L, Goossens A (2011) The JAZ proteins: a crucial interface in the jasmonate signaling cascade. Plant Cell 23(9):3089–3100. 10.1105/tpc.111.089300 DOI: 10.1105/tpc.111.089300
Pecher P, Eschen-Lippold L, Herklotz S, Kuhle K, Naumann K, Bethke G et al (2014) The Arabidopsis thaliana mitogen-activated protein kinases MPK3 and MPK6 target a subclass of ‘VQ-motif’-containing proteins to regulate immune responses. New Phytol 203(2):592–606. 10.1111/nph.12817 DOI: 10.1111/nph.12817
Peng X, Xiao TA, Meng JA, Tao ZA, Zhou D, Tang X et al (2020) Differential expression of rice valine-qlutamine gene family in response to nitric oxide and regulatory circuit of OsVQ7 and OsWRKY24. Rice Sci 27(1):10–20. 10.1016/j.rsci.2019.12.002 DOI: 10.1016/j.rsci.2019.12.002
Perruc E, Charpenteau M, Ramirez BC, Jauneau A, Galaud JP, Ranjeva R et al (2004) A novel calmodulin-binding protein functions as a negative regulator of osmotic stress tolerance in Arabidopsis thaliana seedlings. Plant J 38(3):410–420. 10.1111/j.1365-313X.2004.02062.x DOI: 10.1111/j.1365-313X.2004.02062.x
Petersen K, Qiu JL, Lütje J, Fiil BK, Hansen S, Mundy J et al (2010) Arabidopsis MKS1 is involved in basal immunity and requires an intact N-terminal domain for proper function. PLoS One 5(12):e14364. 10.1371/journal.pone.0014364 DOI: 10.1371/journal.pone.0014364
Qiu JL, Fiil BK, Petersen K, Nielsen HB, Botanga CJ, Thorgrimsen S et al (2008) Arabidopsis MAP kinase 4 regulates gene expression through transcription factor release in the nucleus. EMBO J 27(16):2214–2221. 10.1038/emboj.2008.147 DOI: 10.1038/emboj.2008.147
Roychoudhury A, Paul S, Basu S (2013) Cross-talk between abscisic acid-dependent and abscisic acid-independent pathways during abiotic stress. Plant Cell Rep 32(7):985–1006. 10.1007/s00299-013-1414-5 DOI: 10.1007/s00299-013-1414-5
Scanlon M, Timmermans M (2013) Growth and development: from genes to networks and a mechanistic understanding of plant development. Curr Opin Plant Biol 16(1):1–4. 10.1016/j.pbi.2013.01.002 DOI: 10.1016/j.pbi.2013.01.002
Schuster M, Eisele S, Armas-Egas L, Kessenbrock T, Kourelis J, Kaiser M (2023) Enhanced late blight resistance by engineering an EpiC2B-insensitive immune protease. Plant Biotechnol J. 10.1111/pbi.14209 DOI: 10.1111/pbi.14209
Senthil-Kumar M, Mysore KS (2013) Nonhost resistance against bacterial pathogens: retrospectives and prospects. Annu Rev Phytopathol 51:407–427. 10.1146/annurev-phyto-082712-102319 DOI: 10.1146/annurev-phyto-082712-102319
Shan N, Xiang Z, Sun J, Zhu Q, Xiao Y, Wang P et al (2021) Genome-wide analysis of valine-glutamine motif-containing proteins related to abiotic stress response in cucumber (Cucumis sativus L.). BMC Plant Biol 21(1):492. 10.1186/s12870-021-03242-9 DOI: 10.1186/s12870-021-03242-9
Shen H, Moon J, Huq E (2005) PIF1 is regulated by light-mediated degradation through the ubiquitin-26S proteasome pathway to optimize photomorphogenesis of seedlings in Arabidopsis. Plant J 44(6):1023–1035. 10.1111/j.1365-313X.2005.02606.x DOI: 10.1111/j.1365-313X.2005.02606.x
Shimono M, Sugano S, Nakayama A, Jiang CJ, Ono K, Toki S et al (2007) Rice WRKY45 plays a crucial role in benzothiadiazole-inducible blast resistance. Plant Cell 19(6):2064–2076. 10.1105/tpc.106.046250 DOI: 10.1105/tpc.106.046250
Si Z, Wang L, Ji Z, Qiao Y, Zhang K, Han J (2023) Genome-wide comparative analysis of the valine glutamine motif containing genes in four Ipomoea species. BMC Plant Biol 23(1):209. 10.1186/s12870-023-04235-6 DOI: 10.1186/s12870-023-04235-6
Skubacz A, Daszkowska-Golec A, Szarejko I (2016) The role and regulation of ABI5 (ABA-insensitive 5) in plant development, abiotic stress responses and phytohormone crosstalk. Front Plant Sci 7:1884. 10.3389/fpls.2016.01884 DOI: 10.3389/fpls.2016.01884
Song W, Zhao H, Zhang X, Lei L, Lai J (2016) Genome-wide identification of VQ motif-containing proteins and their expression profiles under abiotic stresses in maize. Front Plant Sci 6:1177. 10.3389/fpls.2015.01177 DOI: 10.3389/fpls.2015.01177
Song X, Meng X, Guo H, Cheng Q, Jing Y, Chen M et al (2022) Targeting a gene regulatory element enhances rice grain yield by decoupling panicle number and size. Nat Biotechnol 40(9):1403–1411. 10.1038/s41587-022-01281-7 DOI: 10.1038/s41587-022-01281-7
Taj G, Agarwal P, Grant M, Kumar A (2010) MAPK machinery in plants: recognition and response to different stresses through multiple signal transduction pathways. Plant Signal Behav 5(11):1370–1378. 10.4161/psb.5.11.13020 DOI: 10.4161/psb.5.11.13020
Tan J, Wang Y, Dymerski R, Wu Z, Weng Y (2022) Sigma factor binding protein 1 (CsSIB1) is a putative candidate of the major-effect QTL dm5.3 for downy mildew resistance in cucumber (Cucumis sativus). Theor Appl Genet 135(12):4197–4215. 10.1007/s00122-022-04212-x DOI: 10.1007/s00122-022-04212-x
Tian X, Li X, Zhou W, Ren Y, Wang Z, Liu Z et al (2017) Transcription factor OsWRKY53 positively regulates brassinosteroid signaling and plant architecture. Plant Physiol 175(3):1337–1349. 10.1104/pp.17.00946 DOI: 10.1104/pp.17.00946
Tian J, Zhang J, Francis F (2023) Large-scale identification and characterization analysis of VQ family genes in plants, especially gymnosperms. Int J Mol Sci 24:14968. 10.3390/ijms241914968 DOI: 10.3390/ijms241914968
Tunyasuvunakool K, Adler J, Wu Z, Green T, Zielinski M, Žídek A et al (2021) Highly accurate protein structure prediction for the human proteome. Nature 596(7873):590–596. 10.1038/s41586-021-03828-1 DOI: 10.1038/s41586-021-03828-1
Tuteja N (2007) Abscisic acid and abiotic stress signaling. Plant Signal Behav 2(3):135–138. 10.4161/psb.2.3.4156 DOI: 10.4161/psb.2.3.4156
Ueno Y, Yoshida R, Kishi-Kaboshi M, Matsushita A, Jiang CJ, Goto S et al (2013) MAP kinases phosphorylate rice WRKY45. Plant Signal Behav 8(6):e24510. 10.4161/psb.24510 DOI: 10.4161/psb.24510
Uji Y, Kashihara K, Kiyama H, Mochizuki S, Akimitsu K, Gomi K (2019) Jasmonic acid-induced VQ-motif-containing protein OsVQ13 influences the OsWRKY45 signaling pathway and grain size by associating with OsMPK6 in rice. Int J Mol Sci 20(12):2917. 10.3390/ijms20122917 DOI: 10.3390/ijms20122917
Waadt R, Seller CA, Hsu PK, Takahashi Y, Munemasa S, Schroeder JI (2022) Plant hormone regulation of abiotic stress responses. Nat Rev Mol Cell Biol 23(10):680–694. 10.1038/s41580-022-00479-6 DOI: 10.1038/s41580-022-00479-6
Wang D, Zhang Y, Zhang Z, Zhu J, Yu J (2010a) KaKs_Calculator 2.0: a toolkit incorporating gamma-series methods and sliding window strategies. Genom Proteom Bioinform 8(1):77–80. 10.1016/S1672-0229(10)60008-3 DOI: 10.1016/S1672-0229(10)60008-3
Wang A, Garcia D, Zhang H, Feng K, Chaudhury A, Berger F et al (2010b) The VQ motif protein IKU1 regulates endosperm growth and seed size in Arabidopsis. Plant J 63(4):670–679. 10.1111/j.1365-313X.2010.04271.x DOI: 10.1111/j.1365-313X.2010.04271.x
Wang X, Zhang H, Sun G, Jin Y, Qiu L (2014) Identification of active VQ motif-containing genes and the expression patterns under low nitrogen treatment in soybean. Gene 543(2):237–243. 10.1016/j.gene.2014.04.012 DOI: 10.1016/j.gene.2014.04.012
Wang M, Vannozzi A, Wang G, Zhong Y, Corso M, Cavallini E et al (2015a) A comprehensive survey of the grapevine VQ gene family and its transcriptional correlation with WRKY proteins. Front Plant Sci 6:417. 10.3389/fpls.2015.00417 DOI: 10.3389/fpls.2015.00417
Wang H, Hu Y, Pan J, Yu D (2015b) Arabidopsis VQ motif-containing proteins VQ12 and VQ29 negatively modulate basal defense against Botrytis cinerea. Sci Rep 5:14185. 10.1038/srep14185 DOI: 10.1038/srep14185
Wang Y, Liu H, Zhu D, Gao Y, Yan H, Xiang Y (2017) Genome-wide analysis of VQ motif-containing proteins in Moso bamboo (Phyllostachys edulis). Planta 246(1):165–181. 10.1007/s00425-017-2693-9 DOI: 10.1007/s00425-017-2693-9
Wang Y, Jiang Z, Li Z, Zhao Y, Tan W, Liu Z et al (2019) Genome-wide identification and expression analysis of the VQ gene family in soybean (Glycine max). PeerJ 7:e7509. 10.7717/peerj.7509 DOI: 10.7717/peerj.7509
Wang X, Kong L, Zhi P, Chang C (2020) Update on Cuticular wax biosynthesis and its roles in plant disease resistance. Int J Mol Sci 21(15):5514. 10.3390/ijms21155514 DOI: 10.3390/ijms21155514
Wang P, Li J, Zhang Z, Zhang Q, Li X, Xiao J et al (2021) OsVQ1 links rice immunity and flowering via interaction with a mitogen-activated protein kinase OsMPK6. Plant Cell Rep 40(10):1989–1999. 10.1007/s00299-021-02766-6 DOI: 10.1007/s00299-021-02766-6
Wang Z, Gao M, Li Y, Zhang J, Su H, Cao M et al (2022a) The transcription factor SlWRKY37 positively regulates jasmonic acid- and dark-induced leaf senescence in tomato. J Exp Bot 73(18):6207–6225. 10.1093/jxb/erac258 DOI: 10.1093/jxb/erac258
Wang J, Lisanza S, Juergens D, Tischer D, Watson JL, Castro KM et al (2022b) Scaffolding protein functional sites using deep learning. Science 377(6604):387–394. 10.1126/science.abn2100 DOI: 10.1126/science.abn2100
Wang D, Wei L, Liu T, Ma J, Huang K, Guo H et al (2023a) Suppression of ETI by PTI priming to balance plant growth and defense through an MPK3/MPK6-WRKYs-PP2Cs module. Mol Plant 16(5):903–918. 10.1016/j.molp.2023.04.004 DOI: 10.1016/j.molp.2023.04.004
Wang Y, Lu X, Fu Y, Wang H, Yu C, Chu J et al (2023b) Genome-wide identification and expression analysis of VQ gene family under abiotic stress in Coix lacryma-jobi L. BMC Plant Biol 23(1):327. 10.1186/s12870-023-04294-9 DOI: 10.1186/s12870-023-04294-9
Wani SH, Anand S, Singh B, Bohra A, Joshi R (2021) WRKY transcription factors and plant defense responses: latest discoveries and future prospects. Plant Cell Rep 40(7):1071–1085. 10.1007/s00299-021-02691-8 DOI: 10.1007/s00299-021-02691-8
Watson JL, Juergens D, Bennett NR, Trippe BL, Yim J, Eisenach HE et al (2023) De novo design of protein structure and function with RFdiffusion. Nature 620(7976):1089–1100. 10.1038/s41586-023-06415-8 DOI: 10.1038/s41586-023-06415-8
Weyhe M, Eschen-Lippold L, Pecher P, Scheel D, Lee J (2014) Ménage à trois: the complex relationships between mitogen-activated protein kinases, WRKY transcription factors, and VQ-motif-containing proteins. Plant Signal Behav 9(8):e29519. 10.4161/psb.29519 DOI: 10.4161/psb.29519
Wu M, Liu H, Han G, Cai R, Pan F, Xiang Y (2017) A moso bamboo WRKY gene PeWRKY83 confers salinity tolerance in transgenic Arabidopsis plants. Sci Rep 7(1):11721. 10.1038/s41598-017-10795-z DOI: 10.1038/s41598-017-10795-z
Xie YD, Li W, Guo D, Dong J, Zhang Q, Fu Y et al (2010) The Arabidopsis gene SIGMA FACTOR-BINDING PROTEIN 1 plays a role in the salicylate- and jasmonate-mediated defence responses. Plant Cell Environ 33(5):828–839. 10.1111/j.1365-3040.2009.02109.x DOI: 10.1111/j.1365-3040.2009.02109.x
Xing S, Chen K, Zhu H, Zhang R, Zhang H, Li B et al (2020) Fine-tuning sugar content in strawberry. Genome Biol 21(1):230. 10.1186/s13059-020-02146-5 DOI: 10.1186/s13059-020-02146-5
Xu K, Wang P (2022) Genome-wide identification and expression analysis of the VQ gene family in Cucurbita pepo L. PeerJ 10:e12827. 10.7717/peerj.12827 DOI: 10.7717/peerj.12827
Xu R, Duan P, Yu H, Zhou Z, Zhang B, Wang R et al (2018) Control of grain size and weight by the OsMKKK10-OsMKK4-OsMAPK6 signaling pathway in rice. Mol Plant 11(6):860–873. 10.1016/j.molp.2018.04.004 DOI: 10.1016/j.molp.2018.04.004
Xu Y, Lin Q, Li X, Wang F, Chen Z, Wang J et al (2021) Fine-tuning the amylose content of rice by precise base editing of the Wx gene. Plant Biotechnol J 19(1):11–13. 10.1111/pbi.13433 DOI: 10.1111/pbi.13433
Xue P, Zhang L, Fan R, Li Y, Han X, Qi T et al (2023) HvMPK4 phosphorylates HvWRKY1 to enhance its suppression of barley immunity to powdery mildew fungus. J Genet Genomics S1673–8527(23):00115–00117. 10.1016/j.jgg.2023.05.005 DOI: 10.1016/j.jgg.2023.05.005
Yamada K, Yamaguchi K, Shirakawa T, Nakagami H, Mine A, Ishikawa K et al (2016) The Arabidopsis CERK1-associated kinase PBL27 connects chitin perception to MAPK activation. EMBO J 35(22):2468–2483. 10.15252/embj.201694248 DOI: 10.15252/embj.201694248
Yan C, Fan M, Yang M, Zhao J, Zhang W, Su Y et al (2018) Injury activates Ca2+/calmodulin-dependent phosphorylation of JAV1-JAZ8-WRKY51 complex for jasmonate biosynthesis. Mol Cell 70(1):136-149.e7. 10.1016/j.molcel.2018.03.013 DOI: 10.1016/j.molcel.2018.03.013
Yan H, Wang Y, Hu B, Qiu Z, Zeng B, Fan C (2019) Genome-wide characterization, evolution, and expression profiling of VQ gene family in response to phytohormone treatments and abiotic stress in Eucalyptus grandis. Int J Mol Sci 20(7):1765. 10.3390/ijms20071765 DOI: 10.3390/ijms20071765
Yan X, Luo R, Liu X, Hou Z, Pei W, Zhu W et al (2023) Characterization and the comprehensive expression analysis of tobacco valine-glutamine genes in response to trichomes development and stress tolerance. Bot Stud 64(1):18. 10.1186/s40529-023-00376-x DOI: 10.1186/s40529-023-00376-x
Yang T, Poovaiah BW (2003) Calcium/calmodulin-mediated signal network in plants. Trends Plant Sci 8(10):505–512. 10.1016/j.tplants.2003.09.004 DOI: 10.1016/j.tplants.2003.09.004
Yang M, Liu Z, Yu Y, Yang M, Guo L, Han X et al (2023) Genome-wide identification of the valine-glutamine motif containing gene family and the role of VQ25-1 in pollen germination in Brassica oleracea. Genes Genomics 45(7):921–934. 10.1007/s13258-023-01375-9 DOI: 10.1007/s13258-023-01375-9
Ye YJ, Xiao YY, Han YC, Shan W, Fan ZQ, Xu QG et al (2016) Banana fruit VQ motif-containing protein5 represses cold-responsive transcription factor MaWRKY26 involved in the regulation of JA biosynthetic genes. Sci Rep 6:23632. 10.1038/srep23632 DOI: 10.1038/srep23632
Yu T, Lu X, Bai Y, Mei X, Guo Z, Liu C et al (2019) Overexpression of the maize transcription factor ZmVQ52 accelerates leaf senescence in Arabidopsis. PLoS One 14(8):e0221949. 10.1371/journal.pone.0221949 DOI: 10.1371/journal.pone.0221949
Yu Z, Duan X, Luo L, Dai S, Ding Z, Xia G (2020) How plant hormones mediate salt stress responses. Trends Plant Sci 25(11):1117–1130. 10.1016/j.tplants.2020.06.008 DOI: 10.1016/j.tplants.2020.06.008
Yuan G, Qian Y, Ren Y, Guan Y, Wu X, Ge C et al (2021) The role of plant-specific VQ motif-containing proteins: an ever-thickening plot. Plant Physiol Biochem 159:12–16. 10.1016/j.plaphy.2020.12.005 DOI: 10.1016/j.plaphy.2020.12.005
Zhang G, Wei B (2019) Characterization of VQ motif-containing protein family and their expression patterns under phytohormones and abiotic stresses in melon (Cucumis melo L.). Plant Growth Regul 89:273–285. 10.1007/s10725-019-00534-x DOI: 10.1007/s10725-019-00534-x
Zhang G, Wang F, Li J, Ding Q, Zhang Y, Li H et al (2015) Genome-wide identification and analysis of the VQ motif-containing protein family in Chinese cabbage (Brassica rapa L. ssp. Pekinensis). Int J Mol Sci 16(12):28683–28704. 10.3390/ijms161226127 DOI: 10.3390/ijms161226127
Zhang H, Si X, Ji X, Fan R, Liu J, Chen K et al (2018) Genome editing of upstream open reading frames enables translational control in plants. Nat Biotechnol 36(9):894–898. 10.1038/nbt.4202 DOI: 10.1038/nbt.4202
Zhang L, Wang K, Han Y, Yan L, Zheng Y, Bi Z et al (2022a) Genome-wide analysis of the VQ motif-containing gene family and expression profiles during phytohormones and abiotic stresses in wheat (Triticum aestivum L.). BMC Genomics 23(1):292. 10.1186/s12864-022-08519-3 DOI: 10.1186/s12864-022-08519-3
Zhang H, Zhang L, Ji Y, Jing Y, Li L, Chen Y et al (2022b) Arabidopsis SIGMA FACTOR BINDING PROTEIN1 (SIB1) and SIB2 inhibit WRKY75 function in abscisic acid-mediated leaf senescence and seed germination. J Exp Bot 73(1):182–196. 10.1093/jxb/erab391 DOI: 10.1093/jxb/erab391
Zhang K, Liu F, Wang Z, Zhuo C, Hu K, Li X et al (2022c) Transcription factor WRKY28 curbs WRKY33-mediated resistance to Sclerotinia sclerotiorum in Brassica napus. Plant Physiol 190(4):2757–2774. 10.1093/plphys/kiac439 DOI: 10.1093/plphys/kiac439
Zhang H, Zhu J, Gong Z, Zhu JK (2022d) Abiotic stress responses in plants. Nat Rev Genet 23(2):104–119. 10.1038/s41576-021-00413-0 DOI: 10.1038/s41576-021-00413-0
Zhang LL, Zheng Y, Xiong XX, Li H, Zhang X, Song YL et al (2023a) The wheat VQ motif-containing protein TaVQ4-D positively regulates drought tolerance in transgenic plants. J Exp Bot 74(18):5591–5605. 10.1093/jxb/erad280 DOI: 10.1093/jxb/erad280
Zhang XW, Xu RR, Liu Y, You CX, An JP (2023b) MdVQ10 promotes wound-triggered leaf senescence in association with MdWRKY75 and undergoes antagonistic modulation of MdCML15 and MdJAZs in apple. Plant J 115(6):1599–1618. 10.1111/tpj.16341 DOI: 10.1111/tpj.16341
Zheng Z, Qamar SA, Chen Z, Mengiste T (2006) Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. Plant J 48(4):592–605. 10.1111/j.1365-313X.2006.02901.x DOI: 10.1111/j.1365-313X.2006.02901.x
Zheng J, Li H, Guo Z, Zhuang X, Huang W, Mao C et al (2022) Comprehensive identification and expression profiling of the VQ motif-containing gene family in Brassica juncea. Biology 11(12):1814. 10.3390/biology11121814 DOI: 10.3390/biology11121814
Zhong Y, Guo C, Chu J, Liu H, Cheng ZM (2018) Microevolution of the VQ gene family in six species of Fragaria. Genome 61(1):49–57. 10.1139/gen-2017-0038 DOI: 10.1139/gen-2017-0038
Zhong Y, Wang P, Zhang X, Cheng ZM (2021) Recent duplications dominate VQ and WRKY gene expansions in six Prunus species. Int J Genomics 2021:4066394. 10.1155/2021/4066394 DOI: 10.1155/2021/4066394
Zhou Y, Yang Y, Zhou X, Chi Y, Fan B, Chen Z (2016) Structural and functional characterization of the VQ protein family and VQ protein variants from soybean. Sci Rep 6:34663. 10.1038/srep34663 DOI: 10.1038/srep34663
Zhou J, Wang X, He Y, Sang T, Wang P, Dai S et al (2020) Differential phosphorylation of the transcription factor WRKY33 by the protein kinases CPK5/CPK6 and MPK3/MPK6 cooperatively regulates camalexin biosynthesis in Arabidopsis. Plant Cell 32(8):2621–2638. 10.1105/tpc.19.00971 DOI: 10.1105/tpc.19.00971
Zhou S, Cai L, Wu H, Wang B, Gu B, Cui S (2023) Fine-tuning rice heading date through multiplex editing of the regulatory regions of key genes by CRISPR-Cas9. Plant Biotechnol J. 10.1111/pbi.14221 DOI: 10.1111/pbi.14221
Zhu H, Zhou Y, Zhai H, He S, Zhao N, Liu Q (2020) A novel sweetpotato WRKY transcription factor, IbWRKY2, positively regulates drought and salt tolerance in transgenic Arabidopsis. Biomolecules 10(4):506. 10.3390/biom10040506 DOI: 10.3390/biom10040506
Zou Z, Liu F, Huang S, Fernando WGD (2021) Genome-wide identification and analysis of the valine-glutamine motif-containing gene family in Brassica napus and functional characterization of BnMKS1 in response to Leptosphaeria maculans. Phytopathology 111(2):281–292. 10.1094/PHYTO-04-20-0134-R DOI: 10.1094/PHYTO-04-20-0134-R