Gene expression shapes the patterns of parallel evolution of herbicide resistance in the agricultural weed<i>Monochoria vaginalis</i>

Tanigaki, Shinji; Uchino, Akira; Okawa, Shinpei; Miura, Chikako; Hamamura, Kenshiro; Matsuo, Mitsuhiro; Yoshino, Namiko; Ueno, Naoya; Toyama, Yusuke; Fukumi, Naoya; Kijima, Eiji; Masuda, Taro; Shimono, Yoshiko; Tominaga, Tohru; Iwakami, Satoshi

doi:10.1101/2021.03.10.434542

Cited by 3 publications

(6 citation statements)

References 66 publications

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“…Taken together, it seems that in C 4 plants, GS1 may be an evolutionary hotspot for mutations that endow glufosinate resistance. Among other factors listed above, the gene expression level itself can be a genome constraint and higher expression can be the driving force for evolution of target site resistance ( Tanigaki et al , 2021 ).…”

Section: Discussionmentioning

confidence: 99%

A naturally evolved mutation (Ser59Gly) in glutamine synthetase confers glufosinate resistance in plants

Chun

Han

et al. 2022

Journal of Experimental Botany

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Glufosinate is an important and widely used non-selective herbicide active on a wide range of plant species. Resistance evolution to glufosinate in weedy plant species (including the global weed Eleusine indica) is underway. Here, we established the molecular basis of target-site glufosinate resistance in Eleusine indica. Full-length E. indica glutamine synthetase (GS) iso-genes (EiGS1-1, 1-2, and 1-3 and EiGS2) were cloned, and expression of EiGS1-1 and EiGS1-2 was higher than EiGS2. A novel point mutation resulting in a Ser-59-Gly substitution in EiGS1-1 was identified in glufosinate-resistant (R) plants. Rice calli and seedlings transformed with the mutant EiGS1-1 gene were resistant to glufosinate. Purified mutant EiGS1-1 expressed in yeast was more tolerant to glufosinate than the wild type (WT) variant. These transgenic results correlate with a more glufosinate-R GS in the crude tissue extract of R versus susceptible E. indica plants. Structural modelling of the mutant EiGS1-1 revealed that the Ser-59 is not directly involved in glufosinate binding but in contact with some important binding residues (e.g. Glu-297) and especially with Asp-56 that forms an intratoroidal contact interface. Importantly, the same Ser-59-Gly mutation was also found in geographically isolated glufosinate-R populations from Malaysia and China, suggesting parallel evolution of this resistance mutation.

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Section: Discussionmentioning

confidence: 99%

A naturally evolved mutation (Ser59Gly) in glutamine synthetase confers glufosinate resistance in plants

Chun

Han

et al. 2022

Journal of Experimental Botany

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Section: Methodsmentioning

confidence: 99%

“…Real-time PCR was performed as described previously (Tanigaki et al ., 2021) using primers listed in Table S1. Some of the primer sets were developed elsewhere (Czechowski et al ., 2005; Iwakami et al ., 2014b; Tanigaki et al ., 2021). Eukaryotic translation initiation factor 4B ( EIF4B ) was used as an internal control gene and data was analyzed by the ΔΔCt method (Schmittgen & Livak, 2008).…”

Section: Methodsmentioning

confidence: 99%

“…Real-time PCR was performed as described previously 49 using primers listed in Table S1. Some of the primer sets were developed elsewhere [49][50][51] . Eukaryotic translation initiation factor 4B (EIF4B)…”

Section: Real-time Pcrmentioning

confidence: 99%

“…Primers used in this study a, Primer concentration in real-time PCR. b, Developed in Tanigaki et al, (2021). c, Developed in Czechowski et al, (2005).…”

Section: Data Availabilitymentioning

confidence: 99%

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Genetically-linked simultaneous overexpression of multiple herbicide-metabolizing genes for broad-spectrum resistance in an agricultural weed Echinochloa phyllopogon

Suda

Kubo

Yoshimoto

et al. 2022

Preprint

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The use of herbicides in agricultural fields has driven the evolution of weeds for resistance, causing a grave threat to the current agriculture. One big mystery of weed resistance involves multiple-herbicide resistance (MHR) concomitant to enhanced herbicide metabolism. Previous research unveiled that the overexpression of catalytically promiscuous cytochrome P450s underlies the metabolism-based cross-resistance in multiple species. However, the concept of activation of promiscuous enzymes does not fully accommodate the resistance to diverse herbicides in MHR Echinochloa phyllopogon although the genetic inheritance of MHR was suggested as under a single gene control. Here, we show that the high-level resistance to diclofop-methyl in E. phyllopogon is caused by the simultaneous overexpression of CYP81A12/21, the previously identified promiscuous P450s, and a novel P450 CYP709C69. We found that the MHR line rapidly produced two distinct hydroxylated-diclofop-acid, only one of which was the major metabolite produced by CYP81As. RNA-seq followed by real-time PCR in the crossed progeny of MHR and sensitive lines identified several P450 genes whose overexpressions were associated with MHR. Gene functional characterization revealed that only CYP709C69 conferred diclofop-methyl resistance in rice calli and produced another hydroxylated-diclofop-acid in yeast, reinforcing the relatively low activity of CYP81As to diclofop-methyl. Plants transformed with CYP709C69 had unchanged sensitivity to 46 herbicides except for clomazone, where transgenic plants became more susceptible. The present findings establish a novel concept that simultaneous overexpression of herbicide-metabolizing genes enhances and broadens the profile of metabolic resistance in weeds.

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A naturally evolved mutation (Ser-59-Gly) in glutamine synthetase confers glufosinate resistance in plants

Zhang,

Yu,

Han

et al. 2024

Preprint

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Glufosinate is an important and widely used non-selective herbicide active on a wide range of plant species. Resistance evolution to glufosinate in weedy plant species (including the global weed Eleusine indica) is underway. Here, we uncover the molecular basis of target-site glufosinate resistance in Eleusine indica. Full-length E. indica glutamine synthetase (GS) iso-genes (EiGS1-1, 1-2, and 1-3 and EiGS2) were cloned, and expression of EiGS1-1 and EiGS1-2 was higher than EiGS2. A novel point mutation resulting in a Ser-59-Gly substitution in EiGS1-1 was identified in glufosinate-resistant (R) plants. Rice calli and seedlings transformed with the mutant EiGS1-1 gene were resistant to glufosinate. Purified yeast recombinant mutant EiGS1-1 was more tolerant to glufosinate than the wild type (WT) variant. These transgenic results correlate with a more glufosinate-R GS in the crude tissue extract of R versus susceptible E. indica plants. Structural modelling of the mutant EiGS1-1 revealed that the Ser-59 is not directly involved in glufosinate binding but in contact with some important binding residues (e.g. Glu-297) and especially with Asp-56 that forms an intratoroidal contact interface. Importantly, the same Ser-59-Gly mutation was also found in geographically isolated glufosinate-R populations from Malaysia and China, suggesting parallel evolution of this resistance mutation.

show abstract

Gene expression shapes the patterns of parallel evolution of herbicide resistance in the agricultural weedMonochoria vaginalis

Cited by 3 publications

References 66 publications

A naturally evolved mutation (Ser59Gly) in glutamine synthetase confers glufosinate resistance in plants

A naturally evolved mutation (Ser59Gly) in glutamine synthetase confers glufosinate resistance in plants

Genetically-linked simultaneous overexpression of multiple herbicide-metabolizing genes for broad-spectrum resistance in an agricultural weed Echinochloa phyllopogon

A naturally evolved mutation (Ser-59-Gly) in glutamine synthetase confers glufosinate resistance in plants

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