Bakkali Y, Ruiz-Santaella JP, Osuna MD, Wagner J, Fischer AJ, De
Prado R. Late watergrass (Echinochloa phyllopogon): mechanisms in
volved in the resistance to fenoxaprop-p-ethyl. J Agric Food Chem.
2007:55(10):4052–4058. https://doi.org/10.1021/jf0624749
Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for
Illumina sequence data. Bioinformatics 2014:30(15):2114–2120.
https://doi.org/10.1093/bioinformatics/btu170
Brazier-Hicks M, Howell A, Cohn J, Hawkes T, Hall G, Mcindoe E,
Edwards R. Chemically induced herbicide tolerance in rice by the
safener metcamifen is associated with a phased stress response. J
Exp Bot. 2020:71(1):411–421. https://doi.org/10.1093/jxb/erz438
Cai L, Comont D, MacGregor D, Lowe C, Beffa R, Neve P, Saski C. The
blackgrass genome reveals patterns of non-parallel evolution of poly
genic herbicide resistance. New Phytol. 2023:237(5):1891–1907.
https://doi.org/10.1111/nph.18655
Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K,
Madden TL. BLAST+: architecture and applications. BMC Bioinformat
ics 2009:10(1):421. https://doi.org/10.1186/1471-2105-10-421
Chayapakdee P. Molecular mechanism of quinclorac resistance in
multiple-Herbicide resistant Echinochloa phyllopogon [PhD thesis.].
[Tsukuba (Japan)] University of Tsukuba; 2019.
Chayapakdee P, Sunohara Y, Endo M, Yamaguchi T, Fan L, Uchino
A, Matsumoto H, Iwakami S. Quinclorac resistance in Echinochloa
phyllopogon is associated with reduced ethylene synthesis rather
than enhanced cyanide detoxification by beta-cyanoalanine
synthase. Pest Manag Sci. 2020:76(4):1195–1204. https://doi.org/10.
1002/ps.5660
Clough SJ, Bent AF. Floral dip: a simplified method for
Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant
J. 1998:16(6):735–743. https://doi.org/10.1046/j.1365-313x.1998.00343.x
Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR.
Genome-wide identification and testing of superior reference genes
for transcript normalization in Arabidopsis. Plant Physiol.
2005:139(1):5–17. https://doi.org/10.1104/pp.105.063743
Délye C. Unravelling the genetic bases of non-target-site-based resist
ance (NTSR) to herbicides: a major challenge for weed science in
the forthcoming decade. Pest Manag Sci. 2013:69(2):176–187.
https://doi.org/10.1002/ps.3318
Dimaano NG, Iwakami S. Cytochrome P450-mediated herbicide me
tabolism in plants: current understanding and prospects. Pest
Manag Sci. 2021:77(1):22–32. https://doi.org/10.1002/ps.6040
Dimaano NG, Yamaguchi T, Fukunishi K, Tominaga T, Iwakami S.
Functional characterization of cytochrome P450 CYP81A subfamily
to disclose the pattern of cross-resistance in Echinochloa phyllopogon.
Plant Mol Biol. 2020:102(4–5):403–416. https://doi.org/10.1007/
s11103-019-00954-3
Ding Y, Weckwerth PR, Poretsky E, Murphy KM, Sims J, Saldivar E,
Christensen SA, Char SN, Yang B, Tong AD, et al. Genetic elucida
tion of interconnected antibiotic pathways mediating maize innate
immunity. Nat Plants. 2020:6(11):1375–1388. https://doi.org/10.
1038/s41477-020-00787-9
Endo M, Iwakami S, Toki S. Precision genome editing in plants via gene
targeting and subsequent break-induced single-strand annealing.
Plant Biotechnol J. 2021:19(3):563–574. https://doi.org/10.1111/pbi.
13485
Fang J, Zhang Y, Liu T, Yan B, Li J, Dong L. Target-site and metabolic
resistance mechanisms to penoxsulam in barnyardgrass (Echinochloa
crus-galli (L.) P. Beauv). J Agric Food Chem. 2019:67(29):8085–8095.
https://doi.org/10.1021/acs.jafc.9b01641
Fischer AJ, Ateh CM, Bayer DE, Hill JE. Herbicide-resistant Echinochloa
oryzoides and E. phyllopogon in California Oryza sativa fields. Weed
Sci. 2000:48(2):225–230. https://doi.org/10.1614/0043-1745(2000)
048[0225:HREOAE]2.0.CO;2
Gaines TA, Duke SO, Morran S, Rigon CAG, Tranel PJ, Kupper A,
Dayan FE. Mechanisms of evolved herbicide resistance. J Biol
Chem. 2020:295(30):10307–10330. https://doi.org/10.1074/jbc.
REV120.013572
Gilchrist CLM, Chooi Y-H. Clinker & clustermap.js: automatic
generation of gene cluster comparison figures. Bioinformatics
2021:37(16):2473–2475. https://doi.org/10.1093/bioinformatics/
btab007
Guo F, Iwakami S, Yamaguchi T, Uchino A, Sunohara Y, Matsumoto
H. Role of CYP81A cytochrome P450s in clomazone metabolism in
Echinochloa phyllopogon. Plant Sci. 2019:283:321–328. https://doi.
org/10.1016/j.plantsci.2019.02.010
Han H, Yu Q, Beffa R, Gonzalez S, Maiwald F, Wang J, Powles SB.
Cytochrome P450 CYP81A10v7 in Lolium rigidum confers metabolic
resistance to herbicides across at least five modes of action. Plant J.
2021:105(1):79–92. https://doi.org/10.1111/tpj.15040
Hofgen R, Willmitzer L. Storage of competent cells for Agrobacterium
transformation. Nucleic Acids Res. 1988:16(20):9877. https://doi.org/
10.1093/nar/16.20.9877
Ito H, Fukuda Y, Murata K, Kimura A. Transformation of intact yeast
cells treated with alkali cations. J Bacteriol. 1983:153(1):163–168.
https://doi.org/10.1128/jb.153.1.163-168.1983
Iwakami S, Endo M, Saika H, Okuno J, Nakamura N, Yokoyama M,
Watanabe H, Toki S, Uchino A, Inamura T. Cytochrome P450
CYP81A12 and CYP81A21 are associated with resistance to two acet
olactate synthase inhibitors in Echinochloa phyllopogon. Plant
Physiol. 2014:165(2):618–629. https://doi.org/10.1104/pp.113.232843
Iwakami S, Kamidate Y, Yamaguchi T, Ishizaka M, Endo M, Suda H,
Nagai K, Sunohara Y, Toki S, Uchino A, et al. CYP81A P450s are
Downloaded from https://academic.oup.com/plphys/advance-article/doi/10.1093/plphys/kiad286/7167345 by Library of Research Reactor Institute, Kyoto University user on 04 August 2023
Supplemental Figure S5. Diclofop-methyl metabolizing
activity of CYP709Cs.
Supplemental Figure S6. Herbicide metabolizing activity
of CYP709C69.
Supplemental Figure S7. Herbicide sensitivity of late
watergrass (E. phyllopogon) in Japan.
Supplemental Figure S8. Annotation correction.
Supplemental Table S1. Primers used in this study.
Supplemental Table S2. The summary of herbicides used
for the functional characterizations of CYP709C69.
Suda et al.
P450 genes in broad-spectrum herbicide resistance
| 3029
Ruiz-Santaella JP, De Prado R, Wagner J, Fischer AJ, Gerhards R.
Resistance mechanisms to cyhalofop-butyl in a biotype of
Echinochloa phyllopogon (Stapf) Koss. from California. J Plant Dis
Prot. 2006:XX:95–100.
Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the com
parative C(T) method. Nat Protoc. 2008:3(6):1101–1108. https://
doi.org/10.1038/nprot.2008.73
Shimabukuro RH, Walsh WC, Hoerauf RA. Metabolism and selectivity
of diclofop-methyl in wild oat and wheat. J Agric Food Chem.
1979:27(3):615–623. https://doi.org/10.1021/jf60223a008
Shimabukuro RH, Walsh WC, Jacobson A. Aryl-O-glucoside of diclo
fop: a detoxication product in wheat shoots and wild oat cell suspen
sion culture. J Agric Food Chem. 1987:35(3):393–397. https://doi.org/
10.1021/jf00075a027
Tanaka FS, Hoffer BL, Shimabukuro RH, Wien RG, Walsh WC.
Identification of the isomeric hydroxylated metabolites of methyl
2-[4-(2, 4-dichlorophenoxy) phenoxy] propanoate (diclofop-methyl)
in wheat. J Agric Food Chem. 1990:38(2):559–565. https://doi.org/10.
1021/jf00092a049
Tanigaki S, Uchino A, Okawa S, Miura C, Hamamura K, Matsuo M,
Yoshino N, Ueno N, Toyama Y, Fukumi N, et al. Gene expression
shapes the patterns of parallel evolution of herbicide resistance in
the agricultural weed Monochoria vaginalis. New Phytol.
2021:232(2):928–940. https://doi.org/10.1111/nph.17624
Toki S. Rapid and efficient Agrobacterium-mediated transformation in
rice. Plant Mol Biol Rep. 1997:15(1):16–21. https://doi.org/10.1007/
BF02772109
Tsuji R, Fischer AJ, Yoshino M, Roel A, Hill JE, Yamasue Y.
Herbicide-resistant late watergrass (Echinochloa phyllopogon): similarity
in morphological and amplified fragment length polymorphism traits.
Weed Sci. 2003:51(5):740–747. https://doi.org/10.1614/P2002-143
Van Etten M, Lee KM, Chang SM, Baucom RS. Parallel and nonparallel
genomic responses contribute to herbicide resistance in Ipomoea
purpurea, a common agricultural weed. PLoS Genet. 2020:16(2):
e1008593. https://doi.org/10.1371/journal.pgen.1008593
Wenger J, Niderman T, Mathew C. Acetyl-CoA carboxylase inhibitors.
In: Krämer W Schirmer U Jeschke P, Matthias W, editors. Modern
crop protection compounds, second, revised and enlarged edition.
Weinheim, Germany: Wiley-VCH; 2012. p. 447–477.
Xu W, Di C, Zhou S, Liu J, Li L, Liu F, Yang X, Ling Y, Su Z. Rice tran
scriptome analysis to identify possible herbicide quinclorac detoxifi
cation genes. Front Genet. 2015:6:306. https://doi.org/10.3389/fgene.
2015.00306
Yamasue Y. Strategy of Echinochloa oryzicola vasing. For survival in
flooded rice. Weed Biol Manag. 2001:1(1):28–36. https://doi.org/10.
1046/j.1445-6664.2001.00008.x
Yan B, Zhang Y, Li J, Fang J, Liu T, Dong L. Transcriptome profiling to
identify cytochrome P450 genes involved in penoxsulam resistance in
Echinochloa glabrescens. Pestic Biochem Physiol. 2019:158:112–120.
https://doi.org/10.1016/j.pestbp.2019.04.017
Yasuor H, Tenbrook PL, Tjeerdema RS, Fischer AJ. Responses to clo
mazone and 5-ketoclomazone by Echinochloa phyllopogon resistant
to multiple herbicides in Californian rice fields. Pest Manag Sci.
2008:64:1031–1039.
Yasuor H, Zou W, Tolstikov VV, Tjeerdema RS, Fischer AJ.
Differential oxidative metabolism and 5-ketoclomazone accumula
tion are involved in Echinochloa phyllopogon resistance to cloma
zone. Plant Physiol. 2010:153:319–326.
Ye CY, Wu D, Mao L, Jia L, Qiu J, Lao S, Chen M, Jiang B, Tang W,
Peng Q, et al. The genomes of the allohexaploid Echinochloa crusgalli and its progenitors provide insights into polyploidization-driven
adaptation. Mol Plant. 2020:13(9):1298–1310. https://doi.org/10.
1016/j.molp.2020.07.001
Yu Q, Powles S. Metabolism-based herbicide resistance and crossresistance in crop weeds: a threat to herbicide sustainability and glo
bal crop production. Plant Physiol. 2014:166(3):1106–1118. https://
doi.org/10.1104/pp.114.242750
Downloaded from https://academic.oup.com/plphys/advance-article/doi/10.1093/plphys/kiad286/7167345 by Library of Research Reactor Institute, Kyoto University user on 04 August 2023
involved in concomitant cross-resistance to acetolactate synthase
and acetyl-CoA carboxylase herbicides in Echinochloa phyllopogon.
New Phytol. 2019:221(4):2112–2122. https://doi.org/10.1111/nph.
15552
Iwakami S, Uchino A, Kataoka Y, Shibaike H, Watanabe H, Inamura
T. Cytochrome P450 genes induced by bispyribac-sodium treatment
in a multiple-herbicide-resistant biotype of Echinochloa phyllopogon.
Pest Manag Sci. 2014:70(4):549–558. https://doi.org/10.1002/ps.3572
Iwakami S, Uchino A, Watanabe H, Yamasue Y, Inamura T. Isolation
and expression of genes for acetolactate synthase and acetyl-CoA
carboxylase in Echinochloa phyllopogon, a polyploid weed species.
Pest Manag Sci. 2012:68(7):1098–1106. https://doi.org/10.1002/ps.
3287
Kandel S, Morant M, Benveniste I, Blee E, Werck-Reichhart D, Pinot
F. Cloning, functional expression, and characterization of CYP709C1,
the first sub-terminal hydroxylase of long chain fatty acid in plants.
Induction by chemicals and methyl jasmonate. J Biol Chem.
2005:280(43):35881–35889. https://doi.org/10.1074/jbc.M500918200
Katoh K, Standley DM. MAFFT Multiple sequence alignment software
version 7: improvements in performance and usability. Mol Biol Evol.
2013:30(4):772–780. https://doi.org/10.1093/molbev/mst010
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular
evolutionary genetics analysis across computing platforms. Mol
Biol Evol. 2018:35(6):1547–1549. https://doi.org/10.1093/molbev/
msy096
Li B, Dewey CN. RSEM: accurate transcript quantification from RNAseq data with or without a reference genome. BMC Bioinformatics
2011:12(1):323. https://doi.org/10.1186/1471-2105-12-323
McFadden JJ, Frear DS, Mansager ER. Aryl hydroxylation of diclofop
by a cytochrome P450 dependent monooxygenase from wheat.
Pestic Biochem Physiol. 1989:34(1):92–100. https://doi.org/10.1016/
0048-3575(89)90145-4
Motohashi K. A simple and efficient seamless DNA cloning method
using SLiCE from Escherichia coli laboratory strains and its application
to SLiP site-directed mutagenesis. BMC Biotechnol. 2015:15(1):47.
https://doi.org/10.1186/s12896-015-0162-8
Murashige T, Skoog F. A revised medium for rapid growth and bio as
says with tobacco tissue cultures. Physiol Plant. 1962:15(3):473–497.
https://doi.org/10.1111/j.1399-3054.1962.tb08052.x
Nandula VK, Riechers DE, Ferhatoglu Y, Barrett M, Duke SO, Dayan
FE, Goldberg-Cavalleri A, Tétard-Jones C, Wortley DJ,
Onkokesung N, et al. Herbicide metabolism: crop selectivity, bioac
tivation, weed resistance, and regulation. Weed Sci. 2019:67(2):
149–175. https://doi.org/10.1017/wsc.2018.88
Owen WJ. Herbicide metabolism as a basis for selectivity. In: Roberts T,
editors. Metabolsim of agrachemicals in plants. Chichester: John
Wiley & Sons Ltd; 2000. p. 211–258.
Pan L, Guo Q, Wang J, Shi L, Yang X, Zhou Y, Yu Q, Bai L. CYP81A68
Confers metabolic resistance to ALS and ACCase-inhibiting herbi
cides and its epigenetic regulation in Echinochloa crus-galli. J
Hazard Mater. 2022:428:128225. https://doi.org/10.1016/j.jhazmat.
2022.128225
Pompon D, Louerat B, Bronine A, Urban P. Yeast expression of animal
and plant P450s in optimized redox environments. Methods Enzymol.
1996:272:51–64. https://doi.org/10.1016/S0076-6879(96)72008-6
Powles SB, Yu Q. Evolution in action: plants resistant to herbicides.
Annu Rev Plant Biol. 2010:61(1):317–347. https://doi.org/10.1146/
annurev-arplant-042809-112119
R Core Team. R: a language and environment for statistical computing.
Vienna, Austria: R Foundation for Statistical Computing; 2022.
Ritz C, Baty F, Streibig JC, Gerhard D. Dose–response analysis using R.
PLoS One 2015:10(12):e0146021. https://doi.org/10.1371/journal.
pone.0146021
Robinson MD, McCarthy DJ, Smyth GK. Edger: a bioconductor
package for differential expression analysis of digital gene expression
data. Bioinformatics 2010:26(1):139–140. https://doi.org/10.1093/
bioinformatics/btp616
PLANT PHYSIOLOGY 2023: 192; 3017–3029
...
論文の公開元へ
