Knockout of the entire family of AITR genes in arabidopsis leads to enhanced drought and salinity tolerance without fitness costs
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BACKGORUND: Environmental stresses including abiotic stresses and biotic stresses limit yield of plants. Stress-tolerant breeding is an efficient way to improve plant yield under stress conditions. Genome editing by CRISPR/Cas9 can be used in molecular breeding to improve agronomic traits in crops, but in most cases, with fitness costs. The plant hormone ABA regulates plant responses to abiotic stresses via signaling transduction. We previously identified AITRs as a family of novel transcription factors that play a role in regulating plant responses to ABA and abiotic stresses. We found that abiotic stress tolerance was increased in the single, double and triple aitr mutants. However, it is unclear if the increased abiotic stress tolerance in the mutants may have fitness costs. RESULTS: We report here the characterization of AITRs as suitable candidate genes for CRISPR/Cas9 editing to improve plant stress tolerance. By using CRISPR/Cas9 to target AITR3 and AITR4 simultaneously in the aitr256 triple and aitr1256 quadruple mutants respectively, we generated Cas9-free aitr23456 quintuple and aitr123456 sextuple mutants. We found that reduced sensitivities to ABA and enhanced tolerance to drought and salt were observed in these mutants. Most importantly, plant growth and development was not affected even in the aitr123456 sextuple mutants, in whom the entire AITR family genes have been knocked out, and the aitr123456 sextuple mutants also showed a wild type response to the pathogen infection. CONCLUSIONS: Our results suggest that knockout of the AITR family genes in Arabidopsis enhanced abiotic stress tolerance without fitness costs. Considering that knock-out a few AITRs will lead to enhanced abiotic stress tolerance, that AITRs are widely distributed in angiosperms with multiple encoding genes, AITRs may be targeted for molecular breeding to improve abiotic stress tolerance in plants including crops.
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Knocking out the AITR gene in Arabidopsis enhanced both drought and salinity tolerance.
“For example, knocking out the AITR gene in Arabidopsis enhanced both drought and salinity tolerance (Chen et al., 2021).”
From Emerging applications of gene editing technologies for the development of climate-resilient crops (2025) · cites this paper as Chen et al., 2021
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Cites
Floral dip: a simplified method for Agrobacterium ‐mediated transformation of Arabidopsis thaliana
Clough, S. J., & Bent, A. F. (1998) · The Plant Journal · doi:10.1046/j.1365-313x.1998.00343.x · Cited by 22,014 · see citing works
A Programmable Dual-RNA–Guided DNA Endonuclease in Adaptive Bacterial Immunity
Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J. A., & Charpentier, E. (2012) · Science · doi:10.1126/science.1225829 · Cited by 17,116 · see citing works
Multiplex Genome Engineering Using CRISPR/Cas Systems
Cong, L., Ran, F. A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P. D., Wu, X., Jiang, W., Marraffini, L. A., et al. (2013) · Science · doi:10.1126/science.1231143 · Cited by 15,339 · see citing works
Plant productivity and environment
Boyer, J. S. (1982) · Science · doi:10.1126/science.218.4571.443 · Cited by 3,959 · see citing works
Wang, W., Vinocur, B. J., & Altman, A. (2003) · Planta · doi:10.1007/s00425-003-1105-5 · Cited by 3,676 · see citing works
Yield trends are insufficient to double global crop production by 2050
Ray, D. K., Mueller, N. D., West, P. C., & Foley, J. A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0066428 · Cited by 3,415 · see citing works
Ma, X., Zhang, Q., Zhu, Q., Liu, W., Chen, Y., Qiu, R., Wang, B., Yang, Z., Li, H., Lin, Y., et al. (2015) · Molecular Plant · doi:10.1016/j.molp.2015.04.007 · Cited by 2,369 · see citing works
Self-citationTargeted genome modification of crop plants using a CRISPR-Cas system
Shan, Q., Wang, Y., Li, J., Zhang, Y., Chen, K., Liang, Z., Zhang, K., Liu, J., Xi, J., Qiu, J., et al. (2013) · Nature Biotechnology · doi:10.1038/nbt.2650 · Cited by 1,965 · see citing works
Fujita, M., Fujita, Y., Noutoshi, Y., Takahashi, F., Narusaka, Y., Yamaguchi‐Shinozaki, K., & Shinozaki, K. (2006) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2006.05.014 · Cited by 1,834 · see citing works
Base editing: precision chemistry on the genome and transcriptome of living cells
Rees, H. A., & Liu, D. R. (2018) · Nature Reviews Genetics · doi:10.1038/s41576-018-0059-1 · Cited by 1,675 · see citing works
CRISPR/Cas Genome Editing and Precision Plant Breeding in Agriculture
Chen, K., Wang, Y., Zhang, R., Zhang, H., & Gao, C. (2019) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-050718-100049 · Cited by 1,643 · see citing works
Evolved Cas9 variants with broad PAM compatibility and high DNA specificity
Hu, J. H., Miller, S. M., Geurts, M. H., Tang, W., Chen, L., Sun, N., Zeina, C. M., Gao, X., Rees, H. A., Lin, Z., et al. (2018) · Nature · doi:10.1038/nature26155 · Cited by 1,552 · see citing works
Li, J., Norville, J. E., Aach, J., McCormack, M., Zhang, D., Bush, J., Church, G. M., & Sheen, J. (2013) · Nature Biotechnology · doi:10.1038/nbt.2654 · Cited by 1,499 · see citing works
CRISPR-Cas guides the future of genetic engineering
Knott, G. J., & Doudna, J. A. (2018) · Science · doi:10.1126/science.aat5011 · Cited by 1,410 · see citing works
Targeted mutagenesis in the model plant Nicotiana benthamiana using Cas9 RNA-guided endonuclease
Nekrasov, V., Staskawicz, B. J., Weigel, D., Jones, J. D. G., & Kamoun, S. (2013) · Nature Biotechnology · doi:10.1038/nbt.2655 · Cited by 1,123 · see citing works
ABA-dependent and ABA-independent signaling in response to osmotic stress in plants
Yoshida, T., Mogami, J., & Yamaguchi‐Shinozaki, K. (2014) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2014.07.009 · Cited by 1,103 · see citing works
Engineered CRISPR-Cas9 nuclease with expanded targeting space
Nishimasu, H., Shi, X., Ishiguro, S., Gao, L., Hirano, S., Okazaki, S., Noda, T., Abudayyeh, O. O., Gootenberg, J. S., Mori, H., et al. (2018) · Science · doi:10.1126/science.aas9129 · Cited by 1,100 · see citing works
Wang, Z.-P., Xing, H.-L., Li, D., Zhang, H.-Y., Han, C.-Y., Wang, X.-C., & Chen, Q.-J. (2015) · Genome biology · doi:10.1186/s13059-015-0715-0 · Cited by 1,036 · see citing works
Molecular Basis of the Core Regulatory Network in ABA Responses: Sensing, Signaling and Transport
Umezawa, T., Nakashima, K., Miyakawa, T., Kuromori, T., Tanokura, M., Shinozaki, K., & Yamaguchi‐Shinozaki, K. (2010) · Plant and Cell Physiology · doi:10.1093/pcp/pcq156 · Cited by 924 · see citing works
Fujii, H., & Zhu, J. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0903144106 · Cited by 885 · see citing works
De novo domestication of wild tomato using genome editing
Zsögön, A., Čermák, T., Naves, E. R., Notini, M. M., Edel, K. H., Weinl, S., Freschi, L., Voytas, D. F., Kudla, J., & Peres, L. E. P. (2018) · Nature Biotechnology · doi:10.1038/nbt.4272 · Cited by 830 · see citing works
Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidine deaminase fusion
Shimatani, Z., Kashojiya, S., Takayama, M., Terada, R., Arazoe, T., Ishii, H., Teramura, H., Yamamoto, T., Komatsu, H., Miura, K., et al. (2017) · Nature Biotechnology · doi:10.1038/nbt.3833 · Cited by 812 · see citing works
Fujii, H., Verslues, P. E., & Zhu, J. (2007) · The Plant Cell · doi:10.1105/tpc.106.048538 · Cited by 733 · see citing works
Fujita, Y., Nakashima, K., Yoshida, T., Katagiri, T., Kidokoro, S., Kanamori, N., Umezawa, T., Fujita, M., Maruyama, K., Ishiyama, K., et al. (2009) · Plant and Cell Physiology · doi:10.1093/pcp/pcp147 · Cited by 733 · see citing works
ABA receptor PYL9 promotes drought resistance and leaf senescence
Zhao, Y., Chan, Z., Gao, J., Lu, X., Cao, M., Yu, C., Hu, Y., You, J., Shi, H., Zhu, Y., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1522840113 · Cited by 700 · see citing works
WRKY transcription factors: key components in abscisic acid signalling
Rushton, D. L., Tripathi, P., Rabara, R., et al. (2011) · Plant Biotechnology Journal · doi:10.1111/j.1467-7652.2011.00634.x · Cited by 693 · see citing works
Yoshida, T., Fujita, Y., Maruyama, K., et al. (2014) · Plant Cell & Environment · doi:10.1111/pce.12351 · Cited by 667 · see citing works
ABI1 Protein Phosphatase 2C Is a Negative Regulator of Abscisic Acid Signaling
Gosti, F., Beaudoin, N., Serizet, C., et al. (1999) · The Plant Cell · doi:10.1105/tpc.11.10.1897 · Cited by 627 · see citing works
Physiological and Molecular Approaches to Improve Drought Resistance in Soybean
Manavalan, L. P., Guttikonda, S. K., Tran, L. P., & Nguyen, H. T. (2009) · Plant and Cell Physiology · doi:10.1093/pcp/pcp082 · Cited by 604 · see citing works
A transcription factor hierarchy defines an environmental stress response network
Song, L., Huang, S. C., Wise, A. S., et al. (2016) · Science · doi:10.1126/science.aag1550 · Cited by 558 · see citing works
A single transcription factor promotes both yield and immunity in rice
Wang, J., Zhou, L., Shi, H., Chern, M., Yu, H. J., Yi, H., He, M., Yin, J., Zhu, X., Li, Y., et al. (2018) · Science · doi:10.1126/science.aat7675 · Cited by 494 · see citing works
Stone, S. L., Williams, L. A., Farmer, L. M., et al. (2006) · The Plant Cell · doi:10.1105/tpc.106.046532 · Cited by 418 · see citing works
uORF-mediated translation allows engineered plant disease resistance without fitness costs
Xu, G., Yuan, M., Ai, C.-R., Liu, L., Zhuang, E., Karapetyan, S., Wang, S., & Dong, X. (2017) · Nature · doi:10.1038/nature22372 · Cited by 393 · see citing works
Self-citationEngineering plants with increased disease resistance: how are we going to express it?
Gurr, S. J., & Rushton, P. J. (2005) · Trends in biotechnology · doi:10.1016/j.tibtech.2005.04.009 · Cited by 327 · see citing works
Degradation of the ABA co-receptor ABI1 by PUB12/13 U-box E3 ligases
Kong, L., Cheng, J., Zhu, Y., Ding, Y., Meng, J., Chen, Z., Xie, Q., Guo, Y., Li, J., Yang, S., et al. (2015) · Nature Communications · doi:10.1038/ncomms9630 · Cited by 316 · see citing works
MYC2 Regulates the Termination of Jasmonate Signaling via an Autoregulatory Negative Feedback Loop
Liu, Y., Du, M., Deng, L., Shen, J., Fang, M., Chen, Q., Lu, Y., Wang, Q., Li, C., & Zhai, Q. (2019) · The Plant Cell · doi:10.1105/tpc.18.00405 · Cited by 312 · see citing works
Berens, M. L., Wolinska, K. W., Spaepen, S., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1817233116 · Cited by 312 · see citing works
Liu, H., & Stone, S. L. (2010) · The Plant Cell · doi:10.1105/tpc.110.076075 · Cited by 298 · see citing works
Abiotic stress responses in plant roots: a proteomics perspective
Ghosh, D., & Xu, J. (2014) · Frontiers in Plant Science · doi:10.3389/fpls.2014.00006 · Cited by 296 · see citing works
Agrochemical control of plant water use using engineered abscisic acid receptors
Park, S., Peterson, F. C., Mosquna, A., Yao, J., Volkman, B. F., & Cutler, S. R. (2015) · Nature · doi:10.1038/nature14123 · Cited by 287 · see citing works
Xu, Z., Kim, S. Y., Hyeon, D. Y., Kim, D. H., Dong, T., Park, Y., Jin, J. B., Joo, S., Kim, S., Hong, J. C., et al. (2013) · The Plant Cell · doi:10.1105/tpc.113.119099 · Cited by 280 · see citing works
Abscisic acid: biosynthesis, inactivation, homoeostasis and signalling
Dong, T., Park, Y., & Hwang, I. (2015) · Essays in Biochemistry · doi:10.1042/bse0580029 · Cited by 275 · see citing works
Bostock, R. M., Pye, M. F., & Roubtsova, T. V. (2014) · Annual Review of Phytopathology · doi:10.1146/annurev-phyto-081211-172902 · Cited by 252 · see citing works
Liu, M., Shi, Z., Zhang, X., Wang, M., Zhang, L., Zheng, K., Liu, J., Hu, X., Di, C., Qian, Q., et al. (2019) · Nature Plants · doi:10.1038/s41477-019-0383-2 · Cited by 252 · see citing works
Gao, X., Chen, J., Dai, X., Zhang, D., & Zhao, Y. (2016) · PLANT PHYSIOLOGY · doi:10.1104/pp.16.00663 · Cited by 246 · see citing works
Valliyodan, B., Ye, H., Song, L., Murphy, M., Shannon, J. G., & Nguyen, H. T. (2016) · Journal of Experimental Botany · doi:10.1093/jxb/erw433 · Cited by 214 · see citing works
He, Y., Zhu, M., Wang, L., et al. (2018) · Molecular Plant · doi:10.1016/j.molp.2018.05.005 · Cited by 203 · see citing works
Bueso, E., Rodríguez, L., Lorenzo‐Orts, L., et al. (2014) · The Plant Journal · doi:10.1111/tpj.12708 · Cited by 197 · see citing works
Belda‐Palazón, B., Rodriguez, L., Fernandez, M. A., Castillo, M.-C., Anderson, E. M., Gao, C., González‐Guzmán, M., Peirats‐Llobet, M., Zhao, Q., Winne, N. D., et al. (2016) · The Plant Cell · doi:10.1105/tpc.16.00178 · Cited by 182 · see citing works
Whole-genome strategies for marker-assisted plant breeding
Xu, Y., Lu, Y., Xie, C., Gao, S., Wan, J., & Prasanna, B. M. (2012) · Molecular Breeding · doi:10.1007/s11032-012-9699-6 · Cited by 173 · see citing works
Seo, K., Lee, J., Nezames, C. D., Zhong, S., Song, E., Byun, M.-O., & Deng, X. W. (2014) · The Plant Cell · doi:10.1105/tpc.113.119974 · Cited by 171 · see citing works
Antiviral Roles of Abscisic Acid in Plants
Alazem, M., & Lin, N. (2017) · Frontiers in Plant Science · doi:10.3389/fpls.2017.01760 · Cited by 159 · see citing works
Huang, Y., Feng, C., Ye, Q., et al. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1005833 · Cited by 153 · see citing works
Chen, Y., Liu, H., Stone, S. L., et al. (2013) · The Plant Journal · doi:10.1111/tpj.12259 · Cited by 132 · see citing works
Yu, F., Lou, L., Tian, M., Li, Q., Ding, Y., Cao, X., Wu, Y., Belda‐Palazón, B., Rodrı́guez, P. L., Yang, S., et al. (2016) · Molecular Plant · doi:10.1016/j.molp.2016.11.002 · Cited by 131 · see citing works
Liu, H., & Stone, S. L. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.465369 · Cited by 129 · see citing works
RACK1 is a negative regulator of ABA responses in Arabidopsis
Guo, J., Wang, J., Xi, L., et al. (2009) · Journal of Experimental Botany · doi:10.1093/jxb/erp221 · Cited by 121 · see citing works
Abscisic Acid Induces Resistance against Bamboo Mosaic Virus through Argonaute 2 and 3
Alazem, M., He, M.-H., Moffett, P., et al. (2017) · PLANT PHYSIOLOGY · doi:10.1104/pp.16.00015 · Cited by 121 · see citing works
Lu, H., Liu, S., Xu, S., Chen, W., Zhou, X., Tan, Y., Huang, J., & Shu, Q. (2017) · Plant Biotechnology Journal · doi:10.1111/pbi.12788 · Cited by 107 · see citing works
Abscisic Acid Receptors: Past, Present and FutureF
Guo, J., Yang, X., Weston, D. J., et al. (2011) · Journal of Integrative Plant Biology · doi:10.1111/j.1744-7909.2011.01044.x · Cited by 105 · see citing works
Rodrı́guez, P. L., Leube, M. P., & Grill, E. (1998) · Plant Molecular Biology · doi:10.1023/a:1006012218704 · Cited by 95 · see citing works
A novel family of transcription factors conserved in angiosperms is required for ABA signalling
Tian, H., Chen, S., Yang, W., Wang, T., Zheng, K., Wang, Y., Cheng, Y., Zhang, N., Liu, S., Li, D., et al. (2017) · Plant Cell & Environment · doi:10.1111/pce.13058 · Cited by 81 · see citing works
Self-citationXun, H., Yang, X., He, H., et al. (2018) · Plant Molecular Biology · doi:10.1007/s11103-018-0804-z · Cited by 77 · see citing works
Tian, H., Guo, H., Dai, X., et al. (2015) · Scientific Reports · doi:10.1038/srep17587 · Cited by 73 · see citing works
Self-citationDai, X., Zhou, L., Zhang, W., et al. (2015) · Plant Cell & Environment · doi:10.1111/pce.12695 · Cited by 71 · see citing works
Kong, Q., Sun, T., Qu, N., Ma, J., Li, M., Cheng, Y.-T., Zhang, Q., Wu, D., Zhang, Z., & Zhang, Y. (2016) · PLANT PHYSIOLOGY · doi:10.1104/pp.15.01954 · Cited by 59 · see citing works
Liu, S., Hu, Q., Luo, S., et al. (2015) · Frontiers in Plant Science · doi:10.3389/fpls.2015.00388 · Cited by 53 · see citing works
Li, X., Xie, Y., Zhu, Q., & Liu, Y. (2017) · Molecular Plant · doi:10.1016/j.molp.2017.10.009 · Cited by 50 · see citing works
Chen, S., Zhang, N., Zhang, Q., Zhou, G., Tian, H., Hussain, S., Ahmed, S., Wang, T., & Wang, S. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20112695 · Cited by 46 · see citing works
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- Authors
- Chen, S., Zhang, N., Zhou, G., Hussain, S., Ahmed, S., Tian, H., & Wang, S.
- Affiliations
- Linyi University (CN)
- Northeast Normal University (CN)
- Corresponding author
- Tian, Hainan
- Wang, Shucai
- Venue
- BMC Plant Biology
- Published
- 2021-03-16
- Volume
- 21
- Issue
- 1
- Pages
- 137-137
- ISSN
- 1471-2229 (ISSN-L)
- PMC
- PMC7967987
- OpenAlex
- W3138213310
- Cited by
- 109
- References
- 69
- Citations by year
- 2026: 19 · 2025: 28 · 2024: 25 · 2023: 21 · 2022: 12 · 2021: 4
- FWCI
- 9.32
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- BMC Plant Biology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Key R&D Program of China (2016YFD0101900)
- Linyi University (LYDX2019BS039)
- National Natural Science Foundation of China (32071938)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Stress Responses and Tolerance
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Seed Germination and Physiology
- Keywords
- abscisic acid signaling, drought tolerance, salt tolerance, abiotic stress tolerance, fitness cost, CRISPR/Cas9 genome editing, gene knockout, Arabidopsis thaliana, pathogen resistance, molecular breeding
- MeSH terms
- Plant Breeding, Stress, Physiological, Transcription Factors, Genes, Plant, Arabidopsis, Gene Expression Regulation, Plant, Gene Silencing, Arabidopsis Proteins, Salinity, Salt Tolerance, Droughts
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