Skip to main content Accessibility help
×
Home

Multiple Herbicide–Resistant Junglerice (Echinochloa colona): Identification of Genes Potentially Involved in Resistance through Differential Gene Expression Analysis

  • Alice A. Wright (a1), Marianela Rodriguez-Carres (a2), Rajkumar Sasidharan (a3), Liisa Koski (a4), Daniel G. Peterson (a5), Vijay K. Nandula (a6), Jeffery D. Ray (a7), Jason A. Bond (a8) and David R. Shaw (a9)...

Abstract

Herbicide resistance, and in particular multiple-herbicide resistance, poses an ever-increasing threat to food security. A biotype of junglerice [Echinochloa colona (L.) Link] with resistance to four herbicides, imazamox, fenoxaprop-P-ethyl, quinclorac, and propanil, each representing a different mechanism of action, was identified in Sunflower County, MS. Dose responses were performed on the resistant biotype and a biotype sensitive to all four herbicides to determine the level of resistance. Application of a cytochrome P450 inhibitor, malathion, with the herbicides imazamox and quinclorac resulted in increased susceptibility in the resistant biotype. Differential gene expression analysis of resistant and sensitive plants revealed that 170 transcripts were upregulated in resistant plants relative to sensitive plants and 160 transcripts were upregulated in sensitive plants. In addition, 507 transcripts were only expressed in resistant plants and 562 only in sensitive plants. A subset of these transcripts were investigated further using quantitative PCR (qPCR) to compare gene expression in resistant plants with expression in additional sensitive biotypes. The qPCR analysis identified two transcripts, a kinase and a glutathione S-transferase that were significantly upregulated in resistant plants compared with the sensitive plants. A third transcript, encoding an F-box protein, was downregulated in the resistant plants relative to the sensitive plants. As no cytochrome P450s were differentially expressed between the resistant and sensitive plants, a single-nucleotide polymorphism analysis was performed, revealing several nonsynonymous point mutations of interest. These candidate genes will require further study to elucidate the resistance mechanisms present in the resistant biotype.

Copyright

Corresponding author

Author for correspondence: Alice A. Wright, Irrigated Agricultural Research and Extension Center, Washington State University, Prosser, WA 99350. (Email: alice.wright@wsu.edu)

References

Hide All
Altop, EK, Mennan, H, Streibig, JC, Budak, U, Ritz, C (2014) Detecting ALS and ACCase herbicide tolerant accession of Echinochloa oryzoides (Ard.) Fritsch. in rice (Oryza sativa L.) fields. Crop Prot 65:202206
An, J, Shen, X, Ma, Q, Yang, C, Liu, S, Chen, Y (2014) Transcriptome profiling to discover putative genes associated with paraquat resistance in goosegrass (Eleusine indica L.). PLoS ONE 9:e99940
Cummins, I, Wortley, DJ, Sabbadin, F, He, Z, Coxon, CR, Straker, HE, Sellars, JD, Knight, K, Edwards, L, Hughes, D, Kaundun, SS, Hutchings, S-J, Steel, PG, Edwards, R (2013) Key role for a glutathione transferase in multiple-herbicide resistance in grass weeds. Proc Natl Acad Sci USA 110:58125817
Duhoux, A, Carrere, S, Gouzy, J, Bonin, L, Delye, C (2015) RNA-Seq analysis of rye-grass transcriptome response to an herbicide inhibiting acetolactate-synthase identifies transcripts linked to non-target-site-based resistance. Plant Mol Biol 87:473487
Fischer, AJ, Bayer, DE, Carrier, MD, Ateh, CM, Yim, K-O (2000) Mechanisms of resistance to bispyribac-sodium in an Echinochloa phyllopogon accession. Pest Biochem Physiol 68:156165
Gaines, TA, Lorentz, L, Figge, A, Herrmann, J, Maiwald, F, Ott, M-C, Han, H, Busi, R, Yu, Q, Powles, SB, Beffa, R (2014) RNA-Seq transcriptome analysis to identify genes involved in metabolism-based diclofop resistance in Lolium rigidum . Plant J 78:865876
Garcia, O, Bouige, P, Forestier, C, Dassa, E (2004) Inventory and comparative analysis of rice and Arabidopsis ATP-binding cassette (ABC) systems. J Mol Biol 343:249265
Gardin, JAC, Gouzy, J, Carrere, S, Delye, C (2015) ALOMYbase, a resource to investigate non-target-site-based resistance to herbicides inhibiting acetolactate-synthase (ALS) in the major grass weed Alopecurus myosuroides (black-grass). BMC Genomics 16:590
Guo, L, Qiu, J, Ye, C, Jin, G, Mao, L, Zhang, H, Yang, X, Pen, Q, Wang, Y, Jia, L, Lin, X, Li, G, Fu, F, Liu, C, Chen, L, Shen, E, Wang, W, Chu, Z, Wu, D, Wu, S, Xia, C, Zhang, Y, Zhou, X, Wang, L, Wu, L, Song, W, Wang, Y, Shu, Q, Aoki, D, Yumot, E, Lou, Y, Qian, Q, Yamaguchi, H, Yamane, H, Kong, C-H, Timko, MP, Bai, L, Fan, L (2017) Echinochloa crus-galli genome analysis provides insight into its adaptation and invasiveness as a weed. Nature Commun 8:1031
Heap, I (2017) The International Survey of Herbicide Resistant Weeds. www.weedscience.org. Accessed: September 29, 2017
Hirase, K, Hoagland, RE (2006) Characterization of aryl acylamidase activity from propanil-resistant barnyardgrass (Echinochloa crus-galli [L.] Beauv.). Weed Biol Manag 6:197203
Iwakami, S, Endo, M, Saika, H, Okuno, J, Nakamura, N, Yokoyama, M, Watanabe, H, Toki, S, Uchino, A, Inamura, T (2014) Cytochrome P450 CYP81A12 and CYP81A21 are associated with resistance to two acetolactate synthase inhibitors in Echinochloa phyllopogon . Plant Physiol 165:618629
Kearse, M, Moir, R, Wilson, A, Stones-Havas, S, Cheung, M, Sturrock, S, Buxton, S, Cooper, A, Markowitz, S, Duran, C, Thierer, T, Ashton, B, Mentjies, P, Drummond, A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:16471649
Leah, JM, Caseley, JC, Riches, CR, Valverde, B (1994) Association between elevated activity of aryl acylamidase and propanil resistance in jungle-rice. Echinochloa colona. Pestic Sci 42:281289
Leslie, T, Baucom, RS (2014) De novo assembly and annotation of the transcriptome of the agricultural weed Ipomoea purpurea uncovers gene expression changes associated with herbicide resistance. G3 4:20352047
Lu, Y-P, Li, Z-S, Drozdowicz, YM, Hortensteiner, S, Martinoia, E, Rea, PA (1998) AtMRP2, an Arabidopsis ATP binding cassette transporter able to transport glutathione S-conjugates and chlorophyll catabolites: functional comparisons with AtMRP1. Plant Cell 10:267282
Muenscher, WC (1955) Weeds. 2nd ed. New York: Macmillan
Pan, G, Zhang, X, Liu, K, Zhang, J, Wu, X, Zhu, J, Tu, J (2006) Map-based cloning of a novel rice cytochrome P450 gene CYP81A6 that confers resistance to two different classes of herbicides. Plant Mol Biol 61:933943
Pan, L, Wang, Z, Cai, J, Gao, H, Zhao, H, Dong, L (2016) High-throughput sequencing reveals differential regulation of miRNAs in fenoxaprop-P-ethyl-resistant Beckmannia syzigachne . Sci Rep 6:28725
Powles, SB, Yu, Q (2010) Evolution in action: plants resistant to herbicides. Annu Rev Plant Biol 61:317347
Rezaei, MK, Shobbar, Z-S, Shahbazi, M, Abedini, R, Zare, S (2013) Glutathione S-transferase (GST) family in barley: identification of members, enzyme activity, and gene expression pattern. J Plant Physiol 170:12771284
Riar, DS, Norsworthy, NK, Srivastava, V, Nandula, V, Bond, JA, Scott, RC (2013) Physiological and molecular basis of acetolactate synthase-inhibiting herbicide resistance in barnyardgrass (Echinochloa crus-galli). J Agric Food Chem 61:278289
Saika, H, Horita, J, Taguchi-Shiobara, F, Nonaka, S, Nishizawa-Yokoi, A, Iwakami, S, Hori, K, Matsumoto, T, Tanaka, T, Itoh, T, Yano, M, Kaku, K, Shimizu, T, Toki, S (2014) A novel rice cytochrome P450 gene, CYP72A31, confers tolerance to acetolactate synthase-inhibiting herbicides in rice and Arabidopsis . Plant Physiol 166:12321240
Sanchez-Fernandez, R, Davies, TGE, Coleman, JOD, Rea, JA (2001) The Arabidopsis thaliana ABC protein superfamily, a complete inventory. J Biol Chem 276:3023130244
Siminszky, B, Sheldon, BS, Corbin, FT, Dewey, RE (2000) A cytochrome P450 monooxygenase cDNA (CYP71A10) confers resistance to linuron in transgenic Nicotiana tabacum . Weed Sci 48:291295
Soranzo, N, Gorla, MS, Mizzi, L, de Toma, G, Frova, C (2004) Organization and structural evolution of the rice glutathione S-transferase gene family. Mol Gen Genomics 271:511521
Stefanowicz, K, Lannoo, N, Van Damme, EJM (2015) Plant F-box proteins—judges between life and death. Crit Rev Plant Sci 34:523552
Tommasini, R, Vogt, E, Fromenteau, M, Hortensteiner, S, Matile, P, Amrhein, N, Martinoia, E (1998) An ABC-transporter of Arabidopsis thaliana has both glutathione-conjugate and chlorophyll catabolite transport activity. Plant J 13:773780
Van Eerd, LL, Hoagland, RE, Zablotowicz, RM, Hall, JC (2003) Pesticide metabolism in plants and microorganisms. Weed Sci 51:472495
Wagner, U, Edwards, R, Dixon, DP, Mauch, F (2002) Probing the diversity of the Arabidopsis glutathione S-transferase gene family. Plant Mol Biol 49:515532
Wright, AA, Nandula, VK, Grier, L, Showmaker, KC, Bond, JA, Peterson, DG, Ray, JD, Shaw, DR (2016) Characterization of fenoxaprop-P-ethyl-resistant junglerice (Echinochloa colona) from Mississippi. Weed Sci 64:588595
Wright, AA, Sasidharan, R, Koski, L, Rodriguez-Carres, M, Peterson, DG, Nandula, VK, Ray, JD, Bond, JA, Shaw, DR (2017) Transcriptomic changes in Echinochloa colona in response to treatment with the herbicide imazamox. Planta 247:369379
Yasour, H, Milan, M, Eckert, JW, Fischer, AJ (2011) Quinclorac resistance: a concerted hormonal and enzymatic effort in Echinochloa phyllopogon . Pest Manag Sci 68:108115
Yih, RY, McRae, DH, Wilson, HF (1968) Mechanism of selective action of 3′, 4′-dichloropopionanilide. Plant Physiol 43:12911296
Yun, M-S, Yogo, Y, Miura, R, Yamasue, Y, Fischer, AJ (2005) Cytochrome P-450 monooxygenase activity in herbicide-resistant and -susceptible late watergrass (Echinochloa phyllopogon). Pestic Biochem Physiol 83:107114
Zulawski, M, Schulze, G, Braginets, R, Hartman, S, Schulze, WX (2014) The Arabidopsis kinome: phylogeny and evolutionary insights into functional diversification. BMC Genomics 15. doi: 10.1186/1471-2164-15-548

Keywords

Type Description Title
PDF
Supplementary materials

Wright et al. supplementary material
Table S1

 PDF (143 KB)
143 KB
PDF
Supplementary materials

Wright et al. supplementary material
Table S2

 PDF (141 KB)
141 KB
PDF
Supplementary materials

Wright et al. supplementary material
Table S3

 PDF (113 KB)
113 KB
PDF
Supplementary materials

Wright et al. supplementary material
Table S4

 PDF (108 KB)
108 KB
PDF
Supplementary materials

Wright et al. supplementary material
Table S5

 PDF (232 KB)
232 KB
PDF
Supplementary materials

Wright et al. supplementary material
Table S6

 PDF (133 KB)
133 KB
PDF
Supplementary materials

Wright et al. supplementary material
Table S7

 PDF (179 KB)
179 KB

Multiple Herbicide–Resistant Junglerice (Echinochloa colona): Identification of Genes Potentially Involved in Resistance through Differential Gene Expression Analysis

  • Alice A. Wright (a1), Marianela Rodriguez-Carres (a2), Rajkumar Sasidharan (a3), Liisa Koski (a4), Daniel G. Peterson (a5), Vijay K. Nandula (a6), Jeffery D. Ray (a7), Jason A. Bond (a8) and David R. Shaw (a9)...

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed