Virus-induced gene silencing of Arabidopsis thaliana gene homologues in wheat identifies genes conferring improved drought tolerance
Open accessAbstract
In a non-model staple crop like wheat (Triticum aestivumI L.), functional validation of potential drought stress responsive genes identified in Arabidopsis could provide gene targets for breeding. Virus-induced gene silencing (VIGS) of genes of interest can overcome the inherent problems of polyploidy and limited transformation potential that hamper functional validation studies in wheat. In this study, three potential candidate genes shown to be involved in abiotic stress response pathways in Arabidopsis thaliana were selected for VIGS experiments in wheat. These include Era1 (enhanced response to abscisic acid), Cyp707a (ABA 8'-hydroxylase), and Sal1 (inositol polyphosphate 1-phosphatase). Gene homologues for these three genes were identified in wheat and cloned in the viral vector barley stripe mosaic virus (BSMV) in the antisense direction, followed by rub inoculation of BSMV viral RNA transcripts onto wheat plants. Quantitative real-time PCR showed that VIGS-treated wheat plants had significant reductions in target gene transcripts. When VIGS-treated plants generated for Era1 and Sal1 were subjected to limiting water conditions, they showed increased relative water content, improved water use efficiency, reduced gas exchange, and better vigour compared to water-stressed control plants inoculated with RNA from the empty viral vector (BSMV0). In comparison, the Cyp707a-silenced plants showed no improvement over BSMV0-inoculated plants under limited water condition. These results indicate that Era1 and Sal1 play important roles in conferring drought tolerance in wheat. Other traits affected by Era1 silencing were also studied. Delayed seed germination in Era1-silenced plants suggests this gene may be a useful target for developing resistance to pre-harvest sprouting.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
VIGS has been used to functionally analyse the Triticum aestivum enhanced response to abscisic acid 1 (TaEra1) and basic transcription factor 3 (TaBTF3) genes in wheat, and inwardly rectifying potassium (K+) channels HvAKT1 and HvAKT2, HVA1, and Hv dehydrin 6 (HvDhn6) genes in barley for drought tolerance.
“VIGS has been used to functionally analyse the Triticum aestivum enhanced response to abscisic acid 1 (TaEra1) and basic transcription factor 3 (TaBTF3) genes in wheat, and inwardly rectifying potassium (K + ) channels HvAKT1 and HvAKT2, HVA1, and Hv dehydrin 6 (HvDhn6) genes in barley for drought tolerance (Liang et al., 2012;Kang et al., 2013;Manmathan et al., 2013;Feng et al., 2020a).”
From Genetic resources and precise gene editing for targeted improvement of barley abiotic stress tolerance (2023) · cites this paper as Manmathan et al., 2013
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
A new mathematical model for relative quantification in real-time RT-PCR
Pfaffl, M. W. (2001) · Nucleic Acids Research · doi:10.1093/nar/29.9.e45 · Cited by 34,610 · see citing works
Primer3 on the WWW for General Users and for Biologist Programmers
Rozen, S., & Skaletsky, H. (2003) · Humana Press eBooks · doi:10.1385/1-59259-192-2:365 · Cited by 14,952 · see citing works
CAP3: A DNA Sequence Assembly Program
Huang, X., & Madan, A. (1999) · Genome Research · doi:10.1101/gr.9.9.868 · Cited by 5,261 · see citing works
Stomatal Conductance and Photosynthesis
Farquhar, G. D., & Sharkey, T. D. (1982) · Annual Review of Plant Physiology · doi:10.1146/annurev.pp.33.060182.001533 · Cited by 4,233 · see citing works
Isotopic Composition of Plant Carbon Correlates With Water-Use Efficiency of Wheat Genotypes
Farquhar, G. D., & Richards, R. A. (1984) · Australian Journal of Plant Physiology · doi:10.1071/pp9840539 · Cited by 2,230 · see citing works
Seki, M., Narusaka, M., Abe, H., Kasuga, M., Yamaguchi‐Shinozaki, K., Carninci, P., Hayashizaki, Y., & Shinozaki, K. (2001) · The Plant Cell · doi:10.1105/tpc.13.1.61 · Cited by 1,105 · see citing works
Genome Plasticity a Key Factor in the Success of Polyploid Wheat Under Domestication
Dubcovsky, J., & Dvořák, J. (2007) · Science · doi:10.1126/science.1143986 · Cited by 1,086 · see citing works
The Arabidopsis cytochrome P450 CYP707A encodes ABA 8′‐hydroxylases: key enzymes in ABA catabolism
Kushiro, T., Okamoto, M., Nakabayashi, K., Yamagishi, K., Kitamura, S., Asami, T., Hirai, N., Koshiba, T., Kamiya, Y., & Nambara, E. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600121 · Cited by 1,022 · see citing works
Breeding for Yield Potential and Stress Adaptation in Cereals
Araus, J., Slafer, G., Royo, C., & Serret, M. (2008) · Critical Reviews in Plant Sciences · doi:10.1080/07352680802467736 · Cited by 804 · see citing works
Genetic Transformation of Wheat Mediated by Agrobacterium tumefaciens
Cheng, M. J., Fry, J. E., Pang, S., Zhou, H., Hironaka, C. M., Duncan, D. R., Conner, T. W., & Wan, Y. (1997) · PLANT PHYSIOLOGY · doi:10.1104/pp.115.3.971 · Cited by 707 · see citing works
Barley stripe mosaic virus ‐induced gene silencing in a monocot plant
Holzberg, S., Brosio, P., Gross, C., & Pogue, G. P. (2002) · The Plant Journal · doi:10.1046/j.1365-313x.2002.01291.x · Cited by 651 · see citing works
Carbon Dioxide and Water Vapor Exchange in Response to Drought in the Atmosphere and in the Soil
Schulze, E. (1986) · Annual Review of Plant Physiology · doi:10.1146/annurev.pp.37.060186.001335 · Cited by 637 · see citing works
Saito, S., Hirai, N., Matsumoto, C., Ohigashi, H., Ohta, D., Sakata, K., & Mizutani, M. (2004) · PLANT PHYSIOLOGY · doi:10.1104/pp.103.037614 · Cited by 568 · see citing works
Genetic and genomic tools to improve drought tolerance in wheat
Fleury, D., Jefferies, S. P., Kuchel, H., & Langridge, P. (2010) · Journal of Experimental Botany · doi:10.1093/jxb/erq152 · Cited by 544 · see citing works
Virus-induced gene silencing in plants
Lu, R. (2003) · Methods · doi:10.1016/s1046-2023(03)00037-9 · Cited by 542 · see citing works
Standardization of real-time PCR gene expression data from independent biological replicates
Willems, E., Leyns, L., & Vandesompele, J. (2008) · Analytical Biochemistry · doi:10.1016/j.ab.2008.04.036 · Cited by 490 · see citing works
Scofield, S. R., Huang, L., Brandt, A. S., & Gill, B. S. (2005) · PLANT PHYSIOLOGY · doi:10.1104/pp.105.061861 · Cited by 480 · see citing works
A Protein Farnesyl Transferase Involved in Abscisic Acid Signal Transduction in Arabidopsis
Cutler, S. R., Ghassemian, M., Bonetta, D. T., Cooney, S., & McCourt, P. (1996) · Science · doi:10.1126/science.273.5279.1239 · Cited by 414 · see citing works
Role of Farnesyltransferase in ABA Regulation of Guard Cell Anion Channels and Plant Water Loss
Pei, Z.-M., Ghassemian, M., Kwak, C. M., McCourt, P., & Schroeder, J. I. (1998) · Science · doi:10.1126/science.282.5387.287 · Cited by 390 · see citing works
Efficient Virus-Induced Gene Silencing in Arabidopsis
Burch‐Smith, T. M., Schiff, M., Liu, Y., & Dinesh-Kumar, S. P. (2006) · PLANT PHYSIOLOGY · doi:10.1104/pp.106.084624 · Cited by 368 · see citing works
Umezawa, T., Okamoto, M., Kushiro, T., Nambara, E., Oono, Y., Seki, M., Kobayashi, M., Koshiba, T., Kamiya, Y., & Shinozaki, K. (2006) · The Plant Journal · doi:10.1111/j.1365-313x.2006.02683.x · Cited by 334 · see citing works
A modified TILLING approach to detect induced mutations in tetraploid and hexaploid wheat
Uauy, C., Paraiso, F., Colasuonno, P., Tran, R. K., Tsai, H., Berardi, S., Comai, L., & Dubcovsky, J. (2009) · BMC Plant Biology · doi:10.1186/1471-2229-9-115 · Cited by 313 · see citing works
Cloutier, S., McCALLUM, B. D., Loutre, C., Banks, T. W., Wicker, T., Feuillet, C., Keller, B., & Jordan, M. C. (2007) · Plant Molecular Biology · doi:10.1007/s11103-007-9201-8 · Cited by 298 · see citing works
Molecular tailoring of farnesylation for plant drought tolerance and yield protection
Wang, Y., Ying, J., Kuzma, M., Chalifoux, M., Sample, A., McArthur, C., Uchacz, T. M., Sarvas, C., Wan, J., Dennis, D. T., et al. (2005) · The Plant Journal · doi:10.1111/j.1365-313x.2005.02463.x · Cited by 250 · see citing works
The nucleotidase/phosphatase SAL1 is a negative regulator of drought tolerance in Arabidopsis
Wilson, P. B., Estavillo, G. M., Field, K. J., Phonphoem, W. P., Carroll, A. J., Howell, K. A., Woo, N. S., Lake, J. A., Smith, S. M., Millar, A. H., et al. (2008) · The Plant Journal · doi:10.1111/j.1365-313x.2008.03780.x · Cited by 198 · see citing works
Quintero, F. J., Garcíadeblas, B., & Rodríguez‐Navarro, A. (1996) · The Plant Cell · doi:10.1105/tpc.8.3.529 · Cited by 196 · see citing works
Aprile, A., Mastrangelo, A. M., Leonardis, A. M. D., Galiba, G., Roncaglia, E., Ferrari, F., Bellis, L. D., Turchi, L., Giuliano, G., & Cattivelli, L. (2009) · BMC Genomics · doi:10.1186/1471-2164-10-279 · Cited by 179 · see citing works
Zhou, H., Biest, N. A., Chen, G., Cheng, M. J., Feng, X., Radionenko, M., Lu, F., Fry, J., Hu, T., Metz, S. G., et al. (2003) · Plant Cell Reports · doi:10.1007/s00299-003-0617-6 · Cited by 176 · see citing works
TILLING moves beyond functional genomics into crop improvement
Slade, A. J., & Knauf, V. C. (2005) · Transgenic Research · doi:10.1007/s11248-005-2770-x · Cited by 159 · see citing works
Zhou, H., Li, S., Deng, Z., Wang, X., Chen, T., Zhang, J., Chen, S., Ling, H., Zhang, A., Wang, D., et al. (2007) · The Plant Journal · doi:10.1111/j.1365-313x.2007.03246.x · Cited by 146 · see citing works
Wang, Y., Beaith, M., Chalifoux, M., Ying, J., Uchacz, T. M., Sarvas, C., Griffiths, R., Kuzma, M., Wan, J., & Huang, Y. (2009) · Molecular Plant · doi:10.1093/mp/ssn088 · Cited by 143 · see citing works
Stability of Barley stripe mosaic virus –Induced Gene Silencing in Barley
Bruun-Rasmussen, M., Madsen, C. T., Jessing, S. G., & Albrechtsen, M. (2007) · Molecular Plant-Microbe Interactions · doi:10.1094/mpmi-20-11-1323 · Cited by 139 · see citing works
Cheng, M. J., Hu, T., Layton, J. G., Liu, C.-N., & Fry, J. E. (2003) · In Vitro Cellular & Developmental Biology - Plant · doi:10.1079/ivp2003471 · Cited by 137 · see citing works
Infectious Barley stripe mosaic virus RNA transcribed in Vitro from full-length genomic cDNA clones
Petty, I. T. D., Hunter, B. G., Wei, N., & Jackson, A. O. (1989) · Virology · doi:10.1016/0042-6822(89)90601-6 · Cited by 129 · see citing works
Allen, G. J., Murata, Y., Chu, S. P., Nafisi, M., & Schroeder, J. I. (2002) · The Plant Cell · doi:10.1105/tpc.010448 · Cited by 117 · see citing works
Lawrence, R. J., & Pikaard, C. S. (2003) · The Plant Journal · doi:10.1046/j.1365-313x.2003.01857.x · Cited by 109 · see citing works
van Eck, L., Schultz, T., Leach, J. E., Scofield, S. R., Peairs, F. B., Botha, A., & Lapitan, N. L. V. (2010) · Plant Biotechnology Journal · doi:10.1111/j.1467-7652.2010.00539.x · Cited by 103 · see citing works
Self-citationAbscisic acid and the pre-harvest sprouting in cereals
Fang, J., & Chu, C. (2008) · Plant Signaling & Behavior · doi:10.4161/psb.3.12.6606 · Cited by 81 · see citing works
A Novel Role for Protein Farnesylation in Plant Innate Immunity
Goritschnig, S., Weihmann, T., Zhang, Y., Fobert, P. R., McCourt, P., & Li, X. (2008) · PLANT PHYSIOLOGY · doi:10.1104/pp.108.117663 · Cited by 78 · see citing works
Mohammadi, M., Kav, N. N. V., & Deyholos, M. K. (2007) · Plant Cell & Environment · doi:10.1111/j.1365-3040.2007.01645.x · Cited by 69 · see citing works
Ekanayake, I. (1993) · Annals of Botany · doi:10.1006/anbo.1993.1082 · Cited by 46 · see citing works
Çakir, C., & Scofield, S. R. (2008) · Cereal Research Communications · doi:10.1556/crc.36.2008.suppl.b.18 · Cited by 29 · see citing works
Variation in genotypic responses and biochemical analysis of callus induction in cultivated wheat
Shah, M. M., Khalid, Q., Khan, U. W., Shah, S. A. H., Shah, S. H., Hassan, A. M. A., & Pervez, A. (2009) · Genetics and Molecular Research · doi:10.4238/vol8-3gmr513 · Cited by 22 · see citing works
Drought-resistant rice for increased rainfed production and poverty alleviation: a concept note
Serraj, R., & Atlin, G. N. (2009) · WORLD SCIENTIFIC eBooks · doi:10.1142/9789814280013_0022 · Cited by 14 · see citing works
Identifying Photoprotection Mutants in Arabidopsis thaliana
Rossel, J. B., Cuttriss, A. J., & Pogson, B. J. (2004) · Humana Press eBooks · doi:10.1385/1-59259-799-8:287 · Cited by 11 · see citing works
Flagged first, then by citations
1 of the 46 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Learning the Languages of the Chloroplast: Retrograde Signaling and Beyond
Chan, K. X., Phua, S. Y., Crisp, P. A., McQuinn, R. P., & Pogson, B. J. (2016) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-043015-111854 · Cited by 583 · see citing works
Drought Tolerance in Modern and Wild Wheat
Budak, H., Kantar, M., & Kurtoğlu, K. Y. (2013) · The Scientific World JOURNAL · doi:10.1155/2013/548246 · Cited by 234 · see citing works
Ogata, T., Ishizaki, T., Fujita, M., & Fujita, Y. (2020) · PLoS ONE · doi:10.1371/journal.pone.0243376 · Cited by 203 · see citing works
Evolution of chloroplast retrograde signaling facilitates green plant adaptation to land
Zhao, C., Wang, Y., Chan, K. X., Marchant, D. B., Franks, P. J., Randall, D., Tee, E. E., Chen, G. J., Ramesh, S. A., Phua, S. Y., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1812092116 · Cited by 193 · see citing works
Chan, K. X., Mabbitt, P. D., Phua, S. Y., Mueller, J. W., Nisar, N., Gigolashvili, T., Ströher, E., Grassl, J., Arlt, W., Estavillo, G. M., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1604936113 · Cited by 184 · see citing works
Cannarozzi, G. M., Plaza‐Wüthrich, S., Esfeld, K., Larti, S., Wilson, Y. S., Girma, D., de Castro, E., Chanyalew, S., Blösch, R., Farinelli, L., et al. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-581 · Cited by 182 · see citing works
Edae, E. A., Byrne, P. F., Manmathan, H. K., Haley, S. D., Moragues, M., Lopes, M. S., & Reynolds, M. P. (2013) · The Plant Genome · doi:10.3835/plantgenome2013.04.0010 · Cited by 171 · see citing works
Self-citationSlNCED1 and SlCYP707A2: key genes involved in ABA metabolism during tomato fruit ripening
Ji, K., Kai, W., Zhao, B., Sun, Y., Yuan, B., Dai, S., Li, Q., Chen, P. C., Wang, Y., Pei, Y., et al. (2014) · Journal of Experimental Botany · doi:10.1093/jxb/eru288 · Cited by 150 · see citing works
Ramegowda, V., Mysore, K. S., & Senthil‐Kumar, M. (2014) · Frontiers in Plant Science · doi:10.3389/fpls.2014.00323 · Cited by 136 · see citing works
The role of retrograde signals during plant stress responses
Crawford, T. S., Lehotai, N., & Strand, Å. (2017) · Journal of Experimental Botany · doi:10.1093/jxb/erx481 · Cited by 135 · see citing works
Sulfation pathways from red to green
Günal, S., Hardman-Kavanaugh, R. E., Kopřiva, S., & Mueller, J. W. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.rev119.007422 · Cited by 117 · see citing works
Chloroplast-to-Nucleus Signaling Regulates MicroRNA Biogenesis in Arabidopsis
Fang, X., Zhao, G., Zhang, S., Li, Y., Gu, H., Li, Y., Zhao, Q. L., & Qi, Y. (2018) · Developmental Cell · doi:10.1016/j.devcel.2018.11.046 · Cited by 115 · see citing works
Los, A., Ziuzina, D., Boehm, D., Cullen, P. J., & Bourke, P. (2019) · Plasma Processes and Polymers · doi:10.1002/ppap.201800148 · Cited by 113 · see citing works
The Role of Abscisic Acid in Drought Stress: How ABA Helps Plants to Cope with Drought Stress
Daszkowska‐Golec, A. (2016) · Springer eBooks · doi:10.1007/978-3-319-32423-4_5 · Cited by 105 · see citing works
Alvarez, S., Choudhury, S. R., & Pandey, S. (2014) · Journal of Proteome Research · doi:10.1021/pr401165b · Cited by 96 · see citing works
Alter, S., Bader, K. C., Spannagl, M., Wang, Y., Bauer, E., Schön, C., & Mayer, K. (2015) · Database · doi:10.1093/database/bav046 · Cited by 88 · see citing works
The advantages of functional phenotyping in pre-field screening for drought-tolerant crops.
Negin, B., & Moshelion, M. (2016) · Functional Plant Biology · doi:10.1071/fp16156 · Cited by 80 · see citing works
Szurman‐Zubrzycka, M., Zbieszczyk, J., Marzec, M., Jelonek, J., Chmielewska, B., Kurowska, M. M., Krok, M., Daszkowska‐Golec, A., Guzy‐Wróbelska, J., Gruszka, D., et al. (2018) · Frontiers in Plant Science · doi:10.3389/fpls.2018.00216 · Cited by 76 · see citing works
Genetic engineering approaches to understanding drought tolerance in plants
Shinwari, Z. K., Jan, S. A., Nakashima, K., & Yamaguchi‐Shinozaki, K. (2020) · Plant Biotechnology Reports · doi:10.1007/s11816-020-00598-6 · Cited by 75 · see citing works
Biotechnological and Digital Revolution for Climate-Smart Plant Breeding
Taranto, F., Nicolia, A., Pavan, S., Vita, P. D., & D’Agostino, N. (2018) · Agronomy · doi:10.3390/agronomy8120277 · Cited by 72 · see citing works
Genome Editing Targets for Improving Nutrient Use Efficiency and Nutrient Stress Adaptation
Sathee, L., Jagadhesan, B., Pandesha, P. H., Barman, D., Adavi, S. B., Nagar, S., Krishna, G. K., Tripathi, S., Jha, S. K., & Chinnusamy, V. (2022) · Frontiers in Genetics · doi:10.3389/fgene.2022.900897 · Cited by 71 · see citing works
Mechanism of ABA signal transduction: Agricultural highlights for improving drought tolerance
Kim, T. (2014) · Journal of Plant Biology · doi:10.1007/s12374-014-0901-8 · Cited by 71 · see citing works
Male sterility systems in wheat and opportunities for hybrid wheat development
Singh, S. P., Srivastava, R., & Kumar, J. (2014) · Acta Physiologiae Plantarum · doi:10.1007/s11738-014-1713-7 · Cited by 67 · see citing works
Chen, K., Li, H., Yaofeng, C., Zheng, Q., Li, B., & Li, Z. (2014) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2014.11.002 · Cited by 61 · see citing works
Billah, M., Aktar, S., Brestič, M., Živčák, M., Khaldun, A. B. M., Uddin, M. S., Bagum, S. A., Yang, X., Skalický, M., Mehari, T. G., et al. (2021) · Plants · doi:10.3390/plants10091910 · Cited by 58 · see citing works
Transgenic cereals: Current status and future prospects
Dunwell, J. M. (2013) · Journal of Cereal Science · doi:10.1016/j.jcs.2013.08.008 · Cited by 57 · see citing works
Wu, J., Wang, L., Lin, Y., Weng, C., Yeh, C.-H., & Wu, S.-J. (2016) · New Phytologist · doi:10.1111/nph.14212 · Cited by 56 · see citing works
Zhao, N., Zhang, Y., Li, Q., Li, R., Xia, X., Qin, X., & Guo, H. (2014) · Plant Physiology and Biochemistry · doi:10.1016/j.plaphy.2014.12.009 · Cited by 55 · see citing works
Dlamini, P. J. (2021) · Plant Stress · doi:10.1016/j.stress.2021.100027 · Cited by 53 · see citing works
Polyploidization: A Biological Force That Enhances Stress Resistance
Li, X., Zhang, L.-Y., Wei, X.-C., Datta, T., Wei, F., & Xie, Z.-P. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25041957 · Cited by 52 · see citing works
Drought stress in maize: stress perception to molecular response and strategies for its improvement
Singh, A. K., Pandey, H., Pandey, S., Lal, D., Chauhan, D., Aparna, Antre, S. H., Santhosh, B., & Kumar, A. (2023) · Functional & Integrative Genomics · doi:10.1007/s10142-023-01226-6 · Cited by 48 · see citing works
Xiao, Z., Xing, M., Liu, X., Fang, Z., Yang, L., Zhang, Y., Wang, Y., Zhuang, M., & Lv, H. (2020) · Planta · doi:10.1007/s00425-020-03454-7 · Cited by 45 · see citing works
CRISPR-Cas9 Gene Editing of the Sal1 Gene Family in Wheat
Mohr, T. J., Horstman, J., Gu, Y., Elarabi, N. I., Abdallah, N. A., & Thilmony, R. L. (2022) · Plants · doi:10.3390/plants11172259 · Cited by 45 · see citing works
Zhang, N., Huo, W., Zhang, L., Chen, F., & Cui, D. (2016) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m115.057232 · Cited by 39 · see citing works
Applications of Virus Induced Gene Silencing (VIGS) in Plant Functional Genomics Studies
Bekele, D., Tesfaye, K., & Fikre, A. (2019) · Journal of Plant Biochemistry & Physiology · doi:10.4172/2329-9029.1000229 · Cited by 39 · see citing works
Zhang, N., Zhang, L., Zhao, L., Ren, Y. N., Cui, D., Chen, J., Wang, Y., Yu, P., & Chen, F. (2017) · Scientific Reports · doi:10.1038/s41598-017-08069-9 · Cited by 37 · see citing works
Ogata, T., Nagatoshi, Y., Yamagishi, N., Yoshikawa, N., & Fujita, Y. (2017) · PLoS ONE · doi:10.1371/journal.pone.0175650 · Cited by 35 · see citing works
Zhang, L., Song, Z., Li, F., Li, X., Ji, H., & Yang, S. (2019) · BMC Plant Biology · doi:10.1186/s12870-019-1948-y · Cited by 33 · see citing works
Retractedde Oliveira, T. M., da Silva, F. R., Bonatto, D., Neves, D. M., Morillón, R., Maserti, B., Filho, M. A. C., Costa, M., Pirovani, C. P., & Gesteira, A. D. S. (2015) · BMC Plant Biology · doi:10.1186/s12870-015-0416-6 · Cited by 30 · see citing works
Wu, J.-R., Wang, T.-Y., Weng, C.-P., Duong, N. K. T., & Wu, S.-J. (2019) · Planta · doi:10.1007/s00425-019-03239-7 · Cited by 29 · see citing works
Daszkowska‐Golec, A., Skubacz, A., Sitko, K., Słota, M., Kurowska, M. M., & Szarejko, I. (2018) · Environmental and Experimental Botany · doi:10.1016/j.envexpbot.2018.01.003 · Cited by 28 · see citing works
Zhang, R., Liu, G., Xu, H., Lou, H., Zhai, S., Chen, A., Hao, S., Xing, J., Liu, J., You, M., et al. (2022) · Journal of Experimental Botany · doi:10.1093/jxb/erac297 · Cited by 26 · see citing works
Milestones achieved in response to drought stress through reverse genetic approaches
Singh, B., Kukreja, S., & Goutam, U. K. (2018) · F1000Research · doi:10.12688/f1000research.15606.1 · Cited by 26 · see citing works
Ahmed, N., Masood, A., Siow, K. S., Wee, M. F. M. R., Auliya, R. Z., & Ho, W. K. (2021) · Agronomy · doi:10.3390/agronomy11020338 · Cited by 23 · see citing works
Niu, F., Bu, Y., Yang, X., Wu, Y., He, M., Zhang, L., & Song, X. (2022) · Journal of Experimental Botany · doi:10.1093/jxb/erac484 · Cited by 22 · see citing works
Tavakol, E. (2017) · Molecular Biotechnology · doi:10.1007/s12033-017-0042-7 · Cited by 21 · see citing works
Measuring Germination Percentage in Wheat
Manmathan, H. K., & Lapitan, N. L. V. (2013) · BIO-PROTOCOL · doi:10.21769/bioprotoc.866 · Cited by 21 · see citing works
Self-citationVIGS: a flexible tool for the study of functional genomics of plants under abiotic stresses
Singh, B., Kukreja, S., Salaria, N., Thakur, K., Gautam, S., Taunk, J., & Goutam, U. K. (2019) · Journal of Crop Improvement · doi:10.1080/15427528.2019.1640821 · Cited by 21 · see citing works
Wang, X., Xu, Y., Li, J., Ren, Y., Wang, Z., Xin, Z., & Lin, T. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19124020 · Cited by 20 · see citing works
Karunarathne, S., Walker, E., Sharma, D., Li, C., & Han, Y. (2023) · Journal of Zhejiang University-SCIENCE B · doi:10.1631/jzus.b2200552 · Cited by 18 · see citing works
“…TaEra1 ) and basic transcription factor 3 ( TaBTF3 ) genes in wheat, and inwardly rectifying potassium (K + ) chan‐ nels HvAKT1 and HvAKT2 , HVA1 , and Hv dehydrin 6 ( HvDhn6 ) genes in barley for drought tolerance (Liang et al., 2012; Kang et al., 2013; Manmathan et al., 2013; Feng et al., 2020a).”
Protein Farnesylation Takes Part in Arabidopsis Seed Development
Vergès, V., Dutilleul, C., Godin, B., Collet, B., Lécureuil, A., Rajjou, L., Guimaraes, C., Pinault, M., Chevalier, S., Giglioli‐Guivarc’h, N., et al. (2021) · Frontiers in Plant Science · doi:10.3389/fpls.2021.620325 · Cited by 17 · see citing works
Amoah, P., Mahamane, A.-R. O., Byiringiro, M. H., Mahula, N. J., Manneh, N., Oluwasegun, Y. R., Assfaw, A. T., Mukiti, H. M., Garba, A. D., Chiemeke, F. K., et al. (2024) · GM crops & food · doi:10.1080/21645698.2024.2411767 · Cited by 18 · see citing works
Bu, Y., Niu, F., He, M., Ye, J., Yang, X., Du, Z., Zhang, L., & Song, X. (2022) · Gene · doi:10.1016/j.gene.2022.146596 · Cited by 16 · see citing works
Bhoite, R. N., Han, Y. N., Chaitanya, A. K., Varshney, R. K., & Sharma, D. L. (2023) · The Plant Genome · doi:10.1002/tpg2.20358 · Cited by 16 · see citing works
Chen, Y., & Xing, Y. (2023) · Plant Cell Reports · doi:10.1007/s00299-023-03040-7 · Cited by 16 · see citing works
Recent Advances on Virus Induced Gene Silencing (VIGS): Plant Functional Genomics
Gupta, B. (2013) · Journal of Plant Biochemistry & Physiology · doi:10.4172/2329-9029.1000e116 · Cited by 15 · see citing works
Calvo-Baltanás, V., Wijnen, C. L., Yang, C., Lukhovitskaya, N., de Snoo, C. B., Hohenwarter, L., Keurentjes, J., de Jong, H., Schnittger, A., & Wijnker, E. (2020) · The Plant Journal · doi:10.1111/tpj.14990 · Cited by 10 · see citing works
Zhang, N., Zhang, L., Shi, C., Zhao, L., Cui, D., & Chen, F. (2018) · Journal of Proteome Research · doi:10.1021/acs.jproteome.7b00745 · Cited by 12 · see citing works
A review on strategies for crop improvement against drought stress through molecular insights
Sharma, A., Dheer, P., Rautela, I., Thapliyal, P. N., Thapliyal, P., Bajpai, A. B., & Sharma, M. D. (2024) · 3 Biotech · doi:10.1007/s13205-024-04020-8 · Cited by 12 · see citing works
Functional Genomics: Applications in Plant Science
Jha, U. C., Bhat, J. S., Patil, B. S., Hossain, F., & Barh, D. (2015) · Springer eBooks · doi:10.1007/978-81-322-2172-2_4 · Cited by 12 · see citing works
Efficient gene editing of a model fern species through gametophyte-based transformation
Jiang, W. J., Deng, F., Babla, M. H., Chen, C., Yang, D., Tong, T., Qin, Y., Chen, G. J., Marchant, D. B., Soltis, P. S., et al. (2024) · PLANT PHYSIOLOGY · doi:10.1093/plphys/kiae473 · Cited by 11 · see citing works
Breeding and Molecular Approaches for Evolving Drought-Tolerant Soybeans
SATPUTE, G. K., Ratnaparkhe, M. B., Chandra, S., Kamble, V. G., Kavishwar, R., Singh, A. K., Gupta, S., Devdas, R., Arya, M., Singh, M., et al. (2020) · Springer eBooks · doi:10.1007/978-981-15-9380-2_4 · Cited by 11 · see citing works
Kumar, J., Kumar, A., Gupta, D. S., Kumar, S., & DePauw, R. M. (2022) · Heredity · doi:10.1038/s41437-022-00513-5 · Cited by 12 · see citing works
Characterization of three chalcone synthase-like genes in Dianthus chinensis
Liu, J., Hao, X.-L., & He, X.-Q. (2021) · Plant Cell Tissue and Organ Culture (PCTOC) · doi:10.1007/s11240-021-02081-8 · Cited by 10 · see citing works
Precision genetic technologies for cereal functional genomics
Liang, Y., Li, C., Mangrauthia, S. K., & Biswal, A. K. (2023) · Journal of Plant Biochemistry and Biotechnology · doi:10.1007/s13562-023-00862-0 · Cited by 9 · see citing works
Nihranz, C. T., Guzchenko, I., & Casteel, C. L. (2023) · Plant Biology · doi:10.1111/plb.13568 · Cited by 8 · see citing works
Crop Biotechnology for Improving Drought Tolerance: Targets, Approaches, and Outcomes
Chater, C., Covarrubias, A. A., & Acosta‐Maspons, A. (2019) · Annual Plant Reviews online · doi:10.1002/9781119312994.apr0669 · Cited by 8 · see citing works
Zhang, L., Song, Z., Li, F., Li, X., Ji, H., & Yang, S. (2020) · BMC Plant Biology · doi:10.1186/s12870-020-02782-w · Cited by 8 · see citing works
RetractedCloning and Characterization of Protein Prenyltransferase Alpha Subunit in Rice
Tao, W., Lou, L., Li, Z., Lianguang, S., & Wang, Q. (2021) · Rice Science · doi:10.1016/j.rsci.2021.05.014 · Cited by 7 · see citing works
Applying Genomics Resources to Accelerate the Development of Climate Resilient Crops
Saini, D. K., Kumar, S., & Kaur, R. (2024) · Springer eBooks · doi:10.1007/978-3-031-28142-6_3 · Cited by 7 · see citing works
Dissecting the Molecular Basis of Drought‐Induced Oxidative Stress Tolerance in Rice
Pradhan, A. K., Jyoti, S. Y., Shandilya, Z. M., Rehman, M., Saikia, D., Poudel, J., Kalita, J., Borborah, K., Chowra, U., Chutia, J., et al. (2021) · doi:10.1002/9781119633174.ch13 · Cited by 7 · see citing works
Virus-Induced Gene Silencing of N Gene in Tobacco by Apple Latent Spherical Virus Vectors
Li, C., & Yoshikawa, N. (2014) · Methods in molecular biology · doi:10.1007/978-1-4939-1743-3_17 · Cited by 6 · see citing works
Shingaliev, A. S., Rekina, A., Gorbachev, M., Dudnikova, K., & Dudnikov, M. (2025) · Horticulturae · doi:10.3390/horticulturae11111297 · Cited by 5 · see citing works
GM Crops for Plant Virus Resistance: A Review
Johnson, A. M. A., Gopal, D. V. R. S., & Sudhakar, C. (2020) · Springer eBooks · doi:10.1007/978-981-15-5932-7_11 · Cited by 5 · see citing works
Zargar, S. M., Nazir, M., Gupta, N., Farhat, S., Mahajan, R., Salgotra, R. K., Rakwal, R., Agrawal, G., & Mir, R. A. (2014) · Molecular Plant Breeding · doi:10.5376/mpb.2014.05.0014 · Cited by 5 · see citing works
Bowerman, A. F., Moore, M., Yadav, A. K., Zhang, J., Mortimer, M. D., Plšková, Z., Tee, E. E., Au, E. K., Collinge, D., Estavillo, G. M., et al. (2025) · New Phytologist · doi:10.1111/nph.70579 · Cited by 4 · see citing works
SAL1 gene: a promising target for improving abiotic stress tolerance in plants a mini review
Elsharawy, H., & Refat, M. (2025) · Physiology and Molecular Biology of Plants · doi:10.1007/s12298-025-01549-7 · Cited by 3 · see citing works
Wang, L., Zhu, Y., Zhao, M., Liu, D., Liao, C., Zhang, H., Gou, Y., & Li, T. (2025) · Frontiers in Plant Science · doi:10.3389/fpls.2025.1647354 · Cited by 2 · see citing works
Combinatorial stress accumulation of wheat small RNAs: Functions and applications
Ros, L. M. D., Kirzinger, M. W. B., Pahari, S., Soolanayakanahally, R. Y., & Kagale, S. (2026) · Plant Stress · doi:10.1016/j.stress.2026.101417 · Cited by 2 · see citing works
Efficient Gene Editing and Overexpression of Gametophyte Transformation in a Model FernPreprint
Jiang, W. J., Deng, F., Babla, M. H., Chen, C., Yang, D., Tong, T., Qin, Y., Chen, G. J., Marchant, D. B., Soltis, P. S., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.04.10.588889 · Cited by 2 · see citing works
Tea Plant Genetic Transformation and Gene Function Research Techniques
Hao, X., Huang, J., Ren, H.-Z., Shi, J., Shen, Y., Zhao, L., & Wang, X. (2024) · Concepts and strategies in plant sciences · doi:10.1007/978-981-97-0680-8_6 · Cited by 1 · see citing works
Impacts of Genome Editing for Abiotic Stress Tolerance in Wheat
Genetu, A., Getahun, T., & Guadie, D. (2025) · Plant Molecular Biology Reporter · doi:10.1007/s11105-025-01621-2 · Cited by 1 · see citing works
Genomic Designing for Abiotic Stress Resistance in Jute
Mitra, J., & Datta, S. (2022) · Springer eBooks · doi:10.1007/978-3-031-05706-9_6 · Cited by 1 · see citing works
Zhang, X., Xia, C., You, S., Chen, Y., Zuo, Y., Zhang, H., Li, W., Zhang, Z., & Deng, H. (2025) · BMC Plant Biology · doi:10.1186/s12870-025-06879-y · Cited by 1 · see citing works
Rapid Induction of Water Stress in Wheat
Manmathan, H. K., & Lapitan, N. L. V. (2013) · BIO-PROTOCOL · doi:10.21769/bioprotoc.867 · Cited by 1 · see citing works
Self-citationSingh, A. K., Kumar, M., Choudhary, D., Rane, J., & Singh, N. P. (2018) · Springer eBooks · doi:10.1007/978-3-319-90650-8_2 · Cited by 1 · see citing works
Kumar, J., Jain, K., Kumari, P., Mohanty, A., Rajani, K., Kumar, R. R., & Ranjan, T. (2020) · IntechOpen eBooks · doi:10.5772/intechopen.92681 · Cited by 1 · see citing works
Flower head development in the Asteraceae family
Zoulias, N. (2014) · Research Explorer (The University of Manchester) · Cited by 1 · see citing works
Serin İklim Tahıllarında Virüs Kaynaklı Gen Susturma: BSMV Kullanımı
İlhan, E., Eren, A., & Erayman, M. (2013) · DergiPark (Istanbul University) · doi:10.17097/zfd.64534
Construction and Functional Identification of VIGS Vector of PDS Gene from Amorphophallus konjac
王, 自. (2018) · Hans Journal of Agricultural Sciences · doi:10.12677/hjas.2018.84060
Probing the function of protein farnesyltransferase in Tripterygium wilfordii
Su, P., Gao, L., Liu, S., Guan, H., Wang, J., Zhang, Y., Zhao, Y., Hu, T., Tu, L., Zhou, J., et al. (2018) · Plant Cell Reports · doi:10.1007/s00299-018-2363-9
Schmidt, R. (2020) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.738709719.793581524
Trends in Arabidopsis Research post genome sequencing- A Scientometric studyPreprint
Kumar, S., Kushwaha, A. K., Thribhuvan, R., Balakrishnan, M., & Krishnan, P. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.02.22.481563
Bowerman, A. F., Moore, M., Yadav, A. K., Zhang, J., Mortimer, M. D., Plšková, Z., Tee, E. E., Au, E. K., Collinge, D., Estavillo, G. M., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.03.10.642515
Azam, A. A., Iqbal, M. S., Saleem, H., Bahitwa, R., & Wang, H. (2026) · Plant Molecular Biology · doi:10.1007/s11103-026-01729-3
Silencing to illuminate: virus-induced gene silencing for accelerated dissection of gene function
Bharati, R., Mogilicherla, K., Dušek, J., Moller, S., Peng, Q., Maruthi, M. N., Moravec, T., Roy, A., & Kundu, J. K. (2026) · Critical Reviews in Plant Sciences · doi:10.1080/07352689.2026.2681404
Sulfur metabolism-dependent retrograde signaling for oxidative stress acclimation
Furbank, R., Plšková, Z., Pogson, B. J., & Chan, K. X. (2026) · Journal of Experimental Botany · doi:10.1093/jxb/erag312
Thirty years of plant farnesylation research: Few substrates, many gaps, and a clear path forward
Daszkowska‐Golec, A., Sundaresan, A. P., & Distefano, M. D. (2026) · Journal of Plant Physiology · doi:10.1016/j.jplph.2026.154887
- Authors
- Manmathan, H., Shaner, D., Snelling, J., Tisserat, N., & Lapitan, N.
- Affiliations
- Colorado State University (US)
- Agricultural Research Service (US)
- Corresponding author
- Lapitan, Nora
- Venue
- Journal of Experimental Botany
- Publisher
- Oxford University Press (OUP)
- Published
- 2013-01-30
- Volume
- 64
- Issue
- 5
- Pages
- 1381-1392
- ISSN
- 0022-0957 (ISSN-L)
- 1460-2431
- PMC
- PMC3598424
- OpenAlex
- W2118469923
- Cited by
- 99
- References
- 46
- Citations by year
- 2026: 5 · 2025: 7 · 2024: 7 · 2023: 6 · 2022: 8 · 2021: 7 · 2020: 10 · 2019: 8 · 2018: 10 · 2017: 4 · 2016: 6 · 2015: 3 · 2014: 11 · 2013: 7
- FWCI
- 10.85
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- cc-by-nc
- Locations
- Journal of Experimental Botany (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Funders
- U.S. Department of Agriculture (2009‐34205‐19960, 2010-34205-21350)
- Colorado State University
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Stress Responses and Tolerance
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Wheat and Barley Genetics and Pathology
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
- Keywords
- virus-induced gene silencing, wheat, drought tolerance, CYP707A, abscisic acid, barley stripe mosaic virus, abiotic stress response, pre-harvest sprouting, seed germination, water use efficiency, homologous genes, functional validation
- MeSH terms
- Adaptation, Physiological, Dehydration, Gases, Mosaic Viruses, Phenotype, Plant Proteins, RNA, Messenger, Seeds, Sequence Homology, Nucleic Acid, Triticum, Genes, Plant, Arabidopsis, Gene Expression Regulation, Plant, Germination, Gene Silencing, Plants, Genetically Modified, Plant Stomata, Droughts, Real-Time Polymerase Chain Reaction
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review