CBF4/DREB1D represses XERICO to attenuate ABA, osmotic and drought stress responses in Arabidopsis.
ABA
Arabidopsis thaliana
CBF4
XERICO
drought stress
osmotic stress
stomata opening
stomatal development
transcriptional regulation
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
05 2022
05 2022
Historique:
revised:
29
01
2022
received:
01
03
2021
accepted:
12
02
2022
pubmed:
25
2
2022
medline:
31
5
2022
entrez:
24
2
2022
Statut:
ppublish
Résumé
Water stress can severely impact plant growth, productivity and yield. Consequently, plants have evolved various strategies through which they can respond and adapt to their environment. XERICO (XER) is a stress-responsive RING E3 ubiquitin ligase that modulates abscisic acid (ABA) levels and promotes drought tolerance when overexpressed. To better understand the biological role of XER in stress responses, we characterized a xer-1 hypomorphic mutant and a CRISPR/Cas9-induced xer-2 null mutant in Arabidopsis. Both xer mutant alleles exhibited increased drought sensitivity, supporting the results from overexpression studies. Furthermore, we discovered that both xer mutants have greater stomatal indices and that XER is expressed in epidermal cells, indicating that XER functions in the epidermis to repress stomatal development. To explore XER spatiotemporal and stress-dependent regulation, we conducted a yeast one-hybrid screen and found that CBF4/DREB1D associates with the XER 5' untranslated region (5'-UTR). We generated three cbf4 null mutants with CRISPR/Cas9 and showed that CBF4 negatively regulates ABA responses, promotes stomatal development and reduces drought tolerance, in contrast to the roles shown for XER. CBF4 is induced by ABA and osmotic stress, and localizes to the nucleus where it downregulates XER expression via the DRE element in its 5'-UTR. Lastly, genetic interaction studies confirmed that xer is epistatic to cbf4 in stomatal development and in ABA, osmotic and drought stress responses. We propose that the repression of XER by CBF4 functions to attenuate ABA signaling and stress responses to maintain a balance between plant growth and survival under adverse environmental conditions.
Substances chimiques
Arabidopsis Proteins
0
CBF4 protein, Arabidopsis
0
Trans-Activators
0
Abscisic Acid
72S9A8J5GW
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
961-977Informations de copyright
© 2022 Society for Experimental Biology and John Wiley & Sons Ltd.
Références
Adrian, J., Chang, J., Ballenger, C.E., Bargmann, B.O.R., Alassimone, J., Davies, K.A. et al. (2015) Transcriptome dynamics of the stomatal lineage: birth, amplification, and termination of a self-renewing population. Developmental Cell, 33, 107-118.
Agarwal, P.K., Gupta, K., Lopato, S. & Agarwal, P. (2017) Dehydration responsive element binding transcription factors and their applications for the engineering of stress tolerance. Journal of Experimental Botany, 68, 2135-2148.
Baas S., Trujillo M. & Lombardi N. (2015) The impact of disasters on agriculture and food security. Food and Agriculture Organization of the United Nations. ISBN 978-92-5-108962-0
Bardou, P., Mariette, J., Escudié, F., Djemiel, C. & Klopp, C. (2014) jvenn: an interactive Venn diagram viewer. BMC Bioinformatics, 15, 293.
Brugière, N., Zhang, W., Xu, Q., Scolaro, E.J., Lu, C., Kahsay, R.Y. et al. (2017) Overexpression of RING domain E3 ligase ZmXerico1 confers drought tolerance through regulation of ABA homeostasis. Plant Physiology, 175, 1350-1369.
Caine, R.S., Yin, X., Sloan, J., Harrison, E.L., Mohammed, U., Fulton, T. et al. (2018) Rice with reduced stomatal density conserves water and has improved drought tolerance under future climate conditions. The New Phytologist, 221, 371-384.
Carianopol, C.S., Chan, A.L., Dong, S., Provart, N.J., Lumba, S. & Gazzarrini, S. (2020) An abscisic acid-responsive protein interaction network for sucrose non-fermenting related kinase1 in abiotic stress response. Communications Biology, 3, 145.
Casson, S.A. & Hetherington, A.M. (2010) Environmental regulation of stomatal development. Current Opinion in Plant Biology, 13, 90-95.
Causier, B., Ashworth, M., Guo, W. & Davies, B. (2012) The TOPLESS interactome: a framework for gene repression in Arabidopsis. Plant Physiology, 158, 423-438.
Chater, C.C.C., Oliver, J., Casson, S. & Gray, J.E. (2014) Putting the brakes on: abscisic acid as a central environmental regulator of stomatal development. The New Phytologist, 202, 376-391.
Chen, I.-C., Huang, I.-C., Liu, M.-J., Wang, Z.-G., Chung, S.-S. & Hsieh, H.-L. (2007) Glutathione S-Transferase Interacting with Far-Red Insensitive 219 Is Involved in Phytochrome A-Mediated Signaling in Arabidopsis. Plant Physiology, 143, 1189-1202.
Chen, K., Li, G.-J., Bressan, R.A., Song, C.-P., Zhu, J.-K. & Zhao, Y. (2020) Abscisic acid dynamics, signaling, and functions in plants. Journal of Integrative Plant Biology, 62, 25-54.
Chow, C.-N., Zheng, H.-Q., Wu, N.-Y., Chien, C.-H., Huang, H.-D., Lee, T.-Y. et al. (2015) PlantPAN 2.0: an update of plant promoter analysis navigator for reconstructing transcriptional regulatory networks in plants. Nucleic Acids Research, 44, D1154-D1160.
Clough, S.J. & Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal, 16, 735-743.
Dong, C.-J. & Liu, J.-Y. (2010) The Arabidopsis EAR-motif-containing protein RAP2.1 functions as an active transcriptional repressor to keep stress responses under tight control. BMC Plant Biology, 10, 47.
Doucet, J., Truong, C., Frank-Webb, E., Lee, H.K., Daneva, A., Gao, Z. et al. (2019) Identification of a role for an E6-like 1 gene in early pollen-stigma interactions in Arabidopsis thaliana. Plant Reproduction, 32, 307-322.
Dow, G.J. & Bergmann, D.C. (2014) Patterning and processes: how stomatal development defines physiological potential. Current Opinion in Plant Biology, 21, 67-74.
Dunn, J., Hunt, L., Afsharinafar, M., Al, M.M., Mitchell, A., Howells, R. et al. (2019) Reduced stomatal density in bread wheat leads to increased water-use efficiency. Journal of Experimental Botany, 70, 4737-4748.
Earley, K.W., Haag, J.R., Pontes, O., Opper, K., Juehne, T., Song, K. et al. (2006) Gateway-compatible vectors for plant functional genomics and proteomics. The Plant Journal, 45, 616-629.
Edgar, R.C. (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics, 5, 113.
Eisele, J.F., Fäßler, F., Bürgel, P.F. & Chaban, C. (2016) A rapid and simple method for microscopy-based stomata analyses. PLoS One, 11, e0164576.
Gaudinier, A., Rodriguez-Medina, J., Zhang, L., Olson, A., Liseron-Monfils, C., Bågman, A.-M. et al. (2018) Transcriptional regulation of nitrogen-associated metabolism and growth. Nature, 563, 259-264.
Gietz, R.D. & Schiestl, R.H. (2007) High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nature Protocols, 2, 31-34.
Gilmour, S.J., Zarka, D.G., Stockinger, E.J., Salazar, M.P., Houghton, J.M. & Thomashow, M.F. (1998) Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. The Plant Journal, 16, 433-442.
Gilmour, S.J., Sebolt, A.M., Salazar, M.P., Everard, J.D. & Thomashow, M.F. (2000) Overexpression of the Arabidopsis CBF3 Transcriptional Activator Mimics Multiple Biochemical Changes Associated with Cold Acclimation. Plant Physiology, 124, 1854-1865.
Gilmour, S.J., Fowler, S.G. & Thomashow, M.F. (2004) Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Plant Molecular Biology, 54, 767-781.
Goda, H., Sasaki, E., Akiyama, K., Maruyama-Nakashita, A., Nakabayashi, K., Li, W. et al. (2008) The AtGenExpress hormone and chemical treatment data set: experimental design, data evaluation, model data analysis and data access. The Plant Journal, 55, 526-542.
Golldack, D., Li, C., Mohan, H. & Probst, N. (2014) Tolerance to drought and salt stress in plants: unraveling the signaling networks. Frontiers in Plant Science, 5, 151.
Gupta, A., Rico-Medina, A. & Caño-Delgado, A.I. (2020) The physiology of plant responses to drought. Science, 368, 266-269.
Guttikonda, S.K., Valliyodan, B., Neelakandan, A.K., Tran, L.-S.P., Kumar, R., Quach, T.N. et al. (2014) Overexpression of AtDREB1D transcription factor improves drought tolerance in soybean. Molecular Biology Reports, 41, 7995-8008.
Haake, V., Cook, D., Riechmann, J., Pineda, O., Thomashow, M.F. & Zhang, J.Z. (2002) Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis. Plant Physiology, 130, 639-648.
Harb, A., Krishnan, A., Ambavaram, M.M.R. & Pereira, A. (2010) Molecular and physiological analysis of drought stress in arabidopsis reveals early responses leading to acclimation in plant growth. Plant Physiology, 154, 1254-1271.
Hellens, R.P., Allan, A.C., Friel, E.N., Bolitho, K., Grafton, K., Templeton, M.D. et al. (2005) Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods, 1, 13.
Hennig, K.M. & Neufeld, T.P. (2002) Inhibition of cellular growth and proliferation by dTOR overexpression in Drosophila. Genesis, 34, 107-110.
Hepworth, C., Doheny-Adams, T., Hunt, L., Cameron, D.D. & Gray, J.E. (2015) Manipulating stomatal density enhances drought tolerance without deleterious effect on nutrient uptake. The New Phytologist, 208, 336-341.
Hetherington, A.M. & Woodward, F.I. (2003) The role of stomata in sensing and driving environmental change. Nature, 424, 901-908.
Higo, K., Ugawa, Y., Iwamoto, M. & Korenaga, T. (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Research, 27, 297-300.
Hirano, T., Matsuzawa, T., Takegawa, K. & Sato, M.H. (2011) Loss-of-function and gain-of-function mutations in FAB1A/B impair endomembrane homeostasis, conferring pleiotropic developmental abnormalities in Arabidopsis. Plant Physiology, 155, 797-807.
Hughes, J., Hepworth, C., Dutton, C., Dunn, J.A., Hunt, L., Stephens, J. et al. (2017) Reducing stomatal density in barley improves drought tolerance without impacting on yield. Plant Physiology, 174, 776-787.
Ito, Y., Katsura, K., Maruyama, K., Taji, T., Kobayashi, M., Seki, M. et al. (2006) Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant & Cell Physiology, 47, 141-153.
Jaglo-Ottosen, K.R., Gilmour, S.J., Zarka, D.G., Schabenberger, O. & Thomashow, M.F. (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science, 280, 104-106.
Jia, Y., Ding, Y., Shi, Y., Zhang, X., Gong, Z. & Yang, S. (2016) The cbfs triple mutants reveal the essential functions of CBFs in cold acclimation and allow the definition of CBF regulons in Arabidopsis. The New Phytologist, 212, 345-353.
Kasuga, M., Liu, Q., Miura, S., Yamaguchi-Shinozaki, K. & Shinozaki, K. (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nature Biotechnology, 17, 287-291.
Kazan, K. (2006) Negative regulation of defence and stress genes by EAR-motif-containing repressors. Trends in Plant Science, 11, 109-112.
Kim, H., Shim, D., Moon, S., Lee, J., Bae, W., Choi, H. et al. (2019) Transcriptional network regulation of the brassinosteroid signaling pathway by the BES1-TPL-HDA19 co-repressor complex. Planta, 250, 1371-1377.
Kim, M.H., Cho, J.S., Park, E.J., Lee, H., Choi, Y.I., Bae, E.K. et al. (2020) Overexpression of a Poplar RING-H2 Zinc Finger, Ptxerico, Confers Enhanced Drought Tolerance via Reduced Water Loss and Ion Leakage in Populus. International Journal of Molecular Sciences, 21, 9454.
Ko, J.H., Yang, S.H. & Han, K.H. (2006) Upregulation of an Arabidopsis RING-H2 gene, XERICO, confers drought tolerance through increased abscisic acid biosynthesis. The Plant Journal, 47, 343-355.
Krogan, N.T., Hogan, K. & Long, J.A. (2012) APETALA2 negatively regulates multiple floral organ identity genes in Arabidopsis by recruiting the co-repressor TOPLESS and the histone deacetylase HDA19. Development, 139, 4180.
Labun, K., Montague, T.G., Gagnon, J.A., Thyme, S.B. & Valen, E. (2016) CHOPCHOP v2: a web tool for the next generation of CRISPR genome engineering. Nucleic Acids Research, 44, W272-W276.
Lata, C. & Prasad, M. (2011) Role of DREBs in regulation of abiotic stress responses in plants. Journal of Experimental Botany, 62, 4731-4748.
Liu, Q., Kasuga, M., Sakuma, Y., Abe, H., Miura, S., Yamaguchi-Shinozaki, K. et al. (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought-and low-temperature-responsive gene expression, respectively, in Arabidopsis. The Plant Cell, 10, 1391-1406.
Liu, X., Yang, S., Zhao, M., Luo, M., Yu, C.-W., Chen, C.-Y. et al. (2014) transcriptional repression by histone deacetylases in plants. Molecular Plant, 7, 764-772.
Long, J.A., Ohno, C., Smith, Z.R. & Meyerowitz, E.M. (2006) TOPLESS regulates apical embryonic fate in Arabidopsis. Science, 312, 1520-1523.
Lumba, S., Toh, S., Handfield, S.F., Swan, M., Liu, R., Youn, J.Y. et al. (2014) A mesoscale abscisic acid hormone interactome reveals a dynamic signaling landscape in Arabidopsis. Developmental Cell, 29, 360-372.
Lynch, T.J., Erickson, B.J., Miller, D.R. & Finkelstein, R.R. (2017) ABI5-binding proteins (AFPs) alter transcription of ABA-induced genes via a variety of interactions with chromatin modifiers. Plant Molecular Biology, 93, 403-418.
Martin-Arevalillo, R., Nanao, M.H., Larrieu, A., Vinos-Poyo, T., Mast, D., Galvan-Ampudia, C. et al. (2017) Structure of the Arabidopsis TOPLESS corepressor provides insight into the evolution of transcriptional repression. Proceedings of the National Academy of Sciences of the United States of America, 114, 8107-8112.
Medina, J., Bargues, M., Terol, J., Pérez-Alonso, M. & Salinas, J. (1999) The Arabidopsis CBF gene family is composed of three genes encoding AP2 domain-containing proteins whose expression is regulated by low temperature but not by abscisic acid or dehydration. Plant Physiology, 119, 463-470.
Medina, J., Catalá, R. & Salinas, J. (2011) The CBFs: three Arabidopsis transcription factors to cold acclimate. Plant Science, 180, 3-11.
Mehdi, S., Derkacheva, M., Ramstrom, M., Kralemann, L., Bergquist, J. & Hennig, L. (2016) The WD40 domain protein MSI1 functions in a histone deacetylase complex to fine-tune abscisic acid signaling. The Plant Cell, 28, 42-54.
Mitsuda, N., Ikeda, M., Takada, S., Takiguchi, Y., Kondou, Y., Yoshizumi, T. et al. (2010) Efficient yeast one-/two-hybrid screening using a library composed only of transcription factors in Arabidopsis thaliana. Plant & Cell Physiology, 51, 2145-2151.
Mizoi, J., Shinozaki, K. & Yamaguchi-Shinozaki, K. (2012) AP2/ERF family transcription factors in plant abiotic stress responses. Biochimica et Biophysica Acta, 1819, 86-96.
Nag, A., Yang, Y. & Jack, T. (2007) DORNRÖSCHEN-LIKE, an AP2 gene, is necessary for stamen emergence in Arabidopsis. Plant Molecular Biology, 65, 219-232.
Nakabayashi, K., Okamoto, M., Koshiba, T., Kamiya, Y. & Nambara, E. (2005) Genome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: epigenetic and genetic regulation of transcription in seed. The Plant Journal, 41, 697-709.
Nakagawa, T., Kurose, T., Hino, T., Tanaka, K., Kawamukai, M., Niwa, Y. et al. (2007) Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. Journal of Bioscience and Bioengineering, 104, 34-41.
Nakano, T., Suzuki, K., Fujimura, T. & Shinshi, H. (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and Rice. Plant Physiology, 140, 411-432.
Nakashima, K. & Yamaguchi-Shinozaki, K. (2013) ABA signaling in stress-response and seed development. Plant Cell Reports, 32, 959-970.
Nemhauser, J.L., Hong, F. & Chory, J. (2006) Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell, 126, 467-475.
Novillo, F., Alonso, J.M., Ecker, J.R. & Salinas, J. (2004) CBF2/DREB1C is a negative regulator of CBF1/DREB1B and CBF3/DREB1A expression and plays a central role in stress tolerance in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 101, 3985-3990.
O'Malley, R.C., Huang, S.C., Song, L., Lewsey, M.G., Bartlett, A., Nery, J.R. et al. (2016) Cistrome and epicistrome features shape the regulatory DNA landscape. Cell, 165, 1280-1292.
Pandey, S., Wang, R.-S., Wilson, L., Li, S., Zhao, Z., Gookin, T.E. et al. (2010) Boolean modeling of transcriptome data reveals novel modes of heterotrimeric G-protein action. Molecular Systems Biology, 6, 372.
Park, S.-Y., Peterson, F.C., Mosquna, A., Yao, J., Volkman, B.F. & Cutler, S.R. (2015) Agrochemical control of plant water use using engineered abscisic acid receptors. Nature, 520, 545-548.
Piñeiro, M., Gómez-Mena, C., Schaffer, R., Martínez-Zapater, J.M. & Coupland, G. (2003) EARLY BOLTING IN SHORT DAYS is related to chromatin remodeling factors and regulates flowering in Arabidopsis by repressing FT. The Plant Cell, 15, 1552-1562.
Prelich, G. (2012) Gene overexpression: uses, mechanisms, and interpretation. Genetics, 190, 841-854.
Pridgeon, A.J. & Hetherington, A.M. (2021) ABA signalling and metabolism are not essential for dark-induced stomatal closure but affect response speed. Scientific Reports, 11, 5751.
Qi, X. & Torii, K.U. (2018) Hormonal and environmental signals guiding stomatal development. BMC Biology, 16, 21.
Ryu, H., Cho, H., Bae, W. & Hwang, I. (2014) Control of early seedling development by BES1/TPL/HDA19-mediated epigenetic regulation of ABI3. Nature Communications, 5, 4138.
Sakuma, Y., Liu, Q., Dubouzet, J.G., Abe, H., Shinozaki, K. & Yamaguchi-Shinozaki, K. (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration-and cold-inducible gene expression. Biochemical and Biophysical Research Communications, 290, 998-1009.
Schmid, M., Davison, T.S., Henz, S.R., Pape, U.J., Demar, M., Vingron, M. et al. (2005) A gene expression map of Arabidopsis thaliana development. Nature Genetics, 37, 501-506.
Schmittgen, T.D. & Livak, K.J. (2008) Analyzing real-time PCR data by the comparative CT method. Nature Protocols, 3, 1101-1108.
Shani, E., Salehin, M., Zhang, Y., Sanchez, S.E., Doherty, C., Wang, R. et al. (2017) Plant stress tolerance requires Auxin-Sensitive Aux/IAA transcriptional repressors. Current Biology, 27, 437-444.
Shin, J., Du, S., Bujdoso, N., Hu, Y. & Davis, S.J. (2013) Overexpression and loss-of-function at TIME FOR COFFEE results in similar phenotypes in diverse growth and physiological responses. Journal of Plant Biology, 56, 152-159.
Song, L., Huang, S.C., Wise, A., Castanon, R., Nery, J.R., Chen, H. et al. (2016) A transcription factor hierarchy defines an environmental stress response network. Science, 354, aag1550.
Sopko, R., Huang, D., Preston, N., Chua, G., Papp, B., Kafadar, K. et al. (2006) Mapping pathways and phenotypes by systematic gene overexpression. Molecular Cell, 21, 319-330.
Tamnanloo, F., Damen, H., Jangra, R. & Lee, J.S. (2018) MAP KINASE PHOSPHATASE1 controls cell fate transition during stomatal development. Plant Physiology, 178, 247-257.
Tanaka, Y., Nose, T., Jikumaru, Y. & Kamiya, Y. (2013) ABA inhibits entry into stomatal-lineage development in Arabidopsis leaves. The Plant Journal, 74, 448-457.
Todaka, D., Shinozaki, K. & Yamaguchi-Shinozaki, K. (2015) Recent advances in the dissection of drought-stress regulatory networks and strategies for development of drought-tolerant transgenic rice plants. Frontiers in Plant Science, 6, 84.
Toufighi, K., Brady, S.M., Austin, R., Ly, E. & Provart, N.J. (2005) the botany array resource: E-Northerns, expression angling, and promoter analyses. The Plant Journal, 43, 153-163.
Tsai, A.Y.-L. & Gazzarrini, S. (2012) Overlapping and distinct roles of AKIN10 and FUSCA3 in ABA and sugar signaling during seed germination. Plant Signaling & Behavior, 7, 1238-1242.
Ueda, M., Matsui, A., Tanaka, M., Nakamura, T., Abe, T., Sako, K. et al. (2017) The distinct roles of Class I and II RPD3-like histone deacetylases in salinity stress response. Plant Physiology, 175, 1760-1773.
Ueda, M., Matsui, A., Nakamura, T., Abe, T., Sunaoshi, Y., Shimada, H. et al. (2018) Versatility of HDA19-deficiency in increasing the tolerance of Arabidopsis to different environmental stresses. Plant Signaling & Behavior, 13, e1475808.
Ueda, M., Matsui, A., Watanabe, S., Kobayashi, M., Saito, K., Tanaka, M. et al. (2019) Transcriptome analysis of the hierarchical response of histone deacetylase proteins that respond in an antagonistic manner to salinity stress. Frontiers in Plant Science, 10, 1323.
Umezawa, T., Sugiyama, N., Takahashi, F., Anderson, J.C., Ishihama, Y., Peck, S.C. et al. (2013) Genetics and phosphoproteomics reveal a protein phosphorylation network in the abscisic acid signaling pathway in Arabidopsis thaliana. Science Signaling, 6, rs8.
Wang, L., Kim, J. & Somers, D.E. (2013) Transcriptional corepressor TOPLESS complexes with pseudoresponse regulator proteins and histone deacetylases to regulate circadian transcription. Proceedings of the National Academy of Sciences of the United States of America, 110, 761-766.
Wang, C., Liu, S., Dong, Y., Zhao, Y., Geng, A., Xia, X. et al. (2016) PdEPF1 regulates water-use efficiency and drought tolerance by modulating stomatal density in poplar. Plant Biotechnology Journal, 14, 849-860.
Wang, Z.-P., Xing, H.-L., Dong, L., Zhang, H.-Y., Han, C.-Y., Wang, X.-C. et al. (2015) Egg cell-specific promoter-controlled CRISPR/Cas9 efficiently generates homozygous mutants for multiple target genes in Arabidopsis in a single generation. Genome Biology, 16, 144.
Xie, Z., Nolan, T.M., Jiang, H. & Yin, Y. (2019) AP2/ERF transcription factor regulatory networks in hormone and abiotic stress responses in Arabidopsis. Frontiers in Plant Science, 10, 228.
Xing, H.-L., Dong, L., Wang, Z.-P., Zhang, H.-Y., Han, C.-Y., Liu, B. et al. (2014) A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biology, 14, 327.
Yamaguchi-Shinozaki, K. & Shinozaki, K. (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annual Review of Plant Biology, 57, 781-803.
Yoshida, T., Fujita, Y., Sayama, H., Kidokoro, S., Maruyama, K., Mizoi, J. et al. (2010) AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. The Plant Journal, 61, 672-685.
Zeng, D.-E., Hou, P., Xiao, F. & Liu, Y. (2013) Overexpression of Arabidopsis XERICO gene confers enhanced drought and salt stress tolerance in rice (Oryza Sativa L.). Journal of Plant Biochemistry and Biotechnology, 24, 56-64.
Zentella, R., Zhang, Z.-L., Park, M., Thomas, S.G., Endo, A., Murase, K. et al. (2007) Global analysis of DELLA direct targets in early gibberellin signaling in Arabidopsis. The Plant Cell, 19, 3037-3057.
Zhao, C., Zhang, Z., Xie, S., Si, T., Li, Y. & Zhu, J.-K. (2016) Mutational evidence for the critical role of CBF transcription factors in cold acclimation in Arabidopsis. Plant Physiology, 171, 2744-2759.
Zhu, Z., Xu, F., Zhang, Y., Cheng, Y.T., Wiermer, M., Li, X. et al. (2010) Arabidopsis resistance protein SNC1 activates immune responses through association with a transcriptional corepressor. Proceedings of the National Academy of Sciences of the United States of America, 107, 13960-13965.