Fitness cost of the Trp-1999-Leu mutation in plastid ACCase on the growth of Beckmannia syzigachne

doi:10.11686/cyxb2023210

Abstract

Abstract:

In this study， we aimed to determine the fitness cost of the Trp-1999-Leu mutation in plastid acetyl co-enzyme A carboxylase （ACCase） on the growth of Beckmannia syzigachne， an important weed of cultivated wheat. The mutant had a homozygous mutation （Leu/Leu， RR） at the 1999 site of ACCase gene’s carboxyl transferase （CT） region， compared with the wild type with Trp/Trp （SS） at the same site. The plant height， aboveground biomass in the early and vegetative stages of growth， fecundity at maturity， and competitiveness with wheat were compared between the wild type and the mutant to clarify the impact of the mutation on the growth of B. syzigachne without herbicide selection pressure. Pot experiments in a greenhouse were conducted to evaluate plant height and aboveground biomass in the early and vegetative stages of growth. The competitiveness of the wild type and the mutant was evaluated using both pot experiments in a greenhouse and field experiments. The results showed that the biomass and plant height of the RR genotype of B. syzigachne were 24.9% and 11.5% lower than that of the SS genotype during 10-15 days of early growth. At the vegetative growth stage， the relative growth rate and net assimilation rate of the RR genotype were 18.2% and 28.6% lower than those of the SS genotype， and the leaf area ratio of the RR genotype was 14.0% higher than that of the SS genotype. However， there was no significant difference in aboveground biomass between the RR and SS genotypes. At the mature stage， the RR genotype allocated less resources to reproductive organs， and the fecundity and total seed weight per plant of the RR genotype were 13.1% and 11.4% lower than their respective values in the SS genotype. In terms of competitiveness， as the density of wheat increased， the aboveground biomass and seed yield of the RR genotype were significantly lower than those of the SS genotype in the greenhouse experiments. This result was confirmed in the field experiment， where the RR genotype showed weaker interspecific competitiveness compared with the SS genotype. Therefore， the ACCase Trp-1999-Leu mutation has significant reproductive and competitive fitness costs in B. syzigachne. These results provide a theoretical basis for the management of this genotype of B. syzigachne.

Key words: Beckmannia syzigachne, acetyl coenzyme A carboxylase, Trp-1999-Leu, fitness cost

Shuang BAI, Qing-hao LYU, Yi-hui LI, Guo-ping LIU, Xiao-yong LUO, Ling-xu LI. Fitness cost of the Trp-1999-Leu mutation in plastid ACCase on the growth of Beckmannia syzigachne[J]. Acta Prataculturae Sinica, 2024, 33(3): 209-216.

Figures/Tables 6

References 28

1	Wang J J， Chen J C， Li X J， et al. Pro-197-Ser mutation in ALS and high-level GST activities： Multiple resistance to ALS and ACCase inhibitors in Beckmannia syzigachne. Frontiers in Plant Science， 2020， 11： 572610.
2	Yan X R， Yang J X， Xue J， et al. Differences in metabolism rate of fenoxaprop-p-ethyl among Beckmannia syzigachne biotypes. Journal of Weed Science，2017， 35（1）： 15-19.
	颜欣茹，杨俊雪，薛君，等. 抗性和敏感生物型菵草代谢精噁唑禾草灵的速度差异. 杂草学报， 2017， 35（1）： 15-19.
3	Lan Y， Li W， Wei S， et al. Multiple resistance to ACCase- and ALS-inhibiting herbicides in black-grass （Alopecurus myosuroides Huds.） in China. Pesticide Biochemistry and Physiology， 2022， 184： 105127.
4	Comont D， Macgregor D R， Crook L， et al. Dissecting weed adaptation： Fitness and trait correlations in herbicide-resistant Alopecurus myosuroides. Pest Management Science， 2022， 78（7）： 3039-3050.
5	Peng Y J. Cyhalofop-butyl-resistance mechanism and herbicide screening of Leptochloa chinensis in rice fields. Changsha： Hunan Agricultural University， 2021.
	彭亚军. 水稻田千金子（Leptochloa chinensis）对氰氟草酯的抗药性机理研究及防除药剂筛选. 长沙：湖南农业大学， 2021.
6	Yin M J， Liu G P， Li Y H， et al. Effects of Trp-1999-Leu mutation in ACCase on seed germination of Beckmannia syzigachne. Shandong Agricultural Sciences， 2021， 53（12）： 44-49.
	尹梦婕，刘国平，李怡慧，等. ACCase Trp-1999-Leu突变对菵草种子萌发的影响. 山东农业科学， 2021， 53（12）： 44-49.
7	Du L. Fitness cost associated with evolved mutant ACCase alleles in American sloughgrass （Beckmannia syzigachne Steud.）. Tai’an： Shandong Agricultural University， 2018.
	杜龙. 基于菵草ACCase等位基因突变的适合度代价研究. 泰安：山东农业大学， 2018.
8	Purrington C B. Costs of resistance. Current Opinion in Plant Biology， 2000， 3： 305-308.
9	Strauss S Y， Rudgers J A， Lau J A， et al. Direct and ecological costs of resistance to herbivory. Trends in Ecology & Evolution， 2002， 17： 278-285.
10	Xu H， Li J， Zhang D， et al. Mutations at codon position 1999 of acetyl-CoA carboxylase confer resistance to ACCase-inhibiting herbicides in Japanese foxtail （Alopecurus japonicus）. Pest Management Science， 2014， 70（12）： 1894-1901.
11	Liu B， Ding F， Wang M， et al. Cross-resistance pattern to ACCase-inhibiting herbicides in a novel Trp1999Leu mutation American sloughgrass （Beckmannia syzigachne） population. Pesticide Biochemistry and Physiology， 2019， 159： 80-84.
12	Hoffmann W A， Poorter H. Avoiding bias in calculations of relative growth rate. Annals of Botany， 2002， 90： 37-42.
13	Poorter H. Plant growth analysis： Towards a synthesis of the classical and the functional approach. Physiologia Plantarum， 1989， 75（2）： 237-244.
14	Reekie E G， Bazzaz F A. Reproductive allocation in plants. California： Elsevier Academic Press， 2005.
15	Vila-aiub M M， Neve P， Powles S B. Evidence for an ecological cost of enhanced herbicide metabolism in Lolium rigidum. Journal of Ecology， 2009， 97（4）： 772-780.
16	Menchari Y， Chauvel B， Darmency H， et al. Fitness costs associated with three mutant acetyl-coenzyme A carboxylase alleles endowing herbicide resistance in black-grass Alopecurus myosuroides. Journal of Applied Ecology， 2007， 45（3）： 939-947.
17	Wang X L， Wang J， Zhang Q L， et al. Fitness of resistant backcross generation （BC3F2-3） between glufosinate-resistant transgenic oilseed rape and wild Brassica juncea. Acta Prataculturae Sinica， 2017， 26（12）： 138-151.
	王晓蕾，王建，张庆玲，等. 抗草甘膦转基因油菜与野荠菜的抗性回交3代子1代和子2代的适合度. 草业学报， 2017， 26（12）： 138-151.
18	Jenczewski E， Ronfort J， Chèvre A M. Crop-to-wild gene flow， introgression and possible fitness effects of transgenes. Environmental Biosafety Research， 2003， 2： 9-24.
19	Warwick S I， Beckie H J， Hall L M. Gene flow， invasiveness， and ecological impact of genetically modified crops. Annals of the New York Academy of Sciences， 2009， 1168（1）： 72-99.
20	Han H， Vila-aiub M M， Jalaludin A， et al. A double EPSPS gene mutation endowing glyphosate resistance shows a remarkably high resistance cost. Plant， Cell & Environment， 2017， 40： 3031-3042.
21	Du L， Qu M J， Jiang X J， et al. Fitness costs associated with acetyl-coenzyme A carboxylase mutations endowing herbicide resistance in American sloughgrass （Beckmannia syzigachne Steud.）. Ecology and Evolution， 2019， 9（4）： 2220-2230.
22	Vila-aiub M M， Yu Q， Han H， et al. Effect of herbicide resistance endowing Ile-1781-Leu and Asp-2078-Gly ACCase gene mutations on ACCase kinetics and growth traits in Lolium rigidum. Journal of Experimental Botany， 2015， 66（15）： 4711-4718.
23	Shergill L S， Boutsalis P， Preston C， et al. Fitness costs associated with 1781 and 2041 ACCase-mutant alleles conferring resistance to herbicides in Hordeum glaucum Steud. Crop Protection， 2016， 87： 60-67.
24	Tang W， Chen J， Yu X， et al. Growth， fecundity， and competition between aryloxyphenoxypropionate-resistant and -susceptible Asia minor bluegrass （Polypogon fugax）. Weed Science， 2019， 67： 546-551.
25	Zhang Y， Xu Y， Wang S， et al. Resistance mutations of Pro197， Asp376 and Trp574 in the acetohydroxyacid synthase （AHAS） affect pigments， growths， and competitiveness of Descurainia sophia L. Scientific Reports， 2017， 7： 16380.
26	Matzrafi M， Gerson O， Rubin B， et al. Different mutations endowing resistance to acetyl-CoA carboxylase inhibitors results in changes in ecological fitness of Lolium rigidum populations. Frontiers in Plant Science， 2017， 8： 1078.
27	Tseng T M， Shrestha S， Mccurdy J D， et al. Target-site mutation and fitness cost of acetolactate synthase inhibitor-resistant annual bluegrass. HortScience， 2019， 54（4）： 701-705.
28	Panozzo S， Scarabel L， Rosan V， et al. A new Ala-122-Asn amino acid change confers decreased fitness to ALS-resistant Echinochloa crus-galli. Frontiers in Plant Science， 2017， 8： 2042.

基因型Genotype	生物量Biomass （g·plant^-1）		株高Plant height （mm）
基因型Genotype	10 d	15 d	10 d	15 d
RR	1.55±0.16	2.05±0.42	48.08±2.93	86.65±6.89
SS	1.35±0.10	2.73±0.55*	50.78±3.16	97.92±5.98*

基因型Genotype	生物量Biomass （g·plant^-1）		株高Plant height （mm）
基因型Genotype	10 d	15 d	10 d	15 d
RR	1.55±0.16	2.05±0.42	48.08±2.93	86.65±6.89
SS	1.35±0.10	2.73±0.55*	50.78±3.16	97.92±5.98*

指标Indicator	RR	SS
分蘖数Tiller number	2.8±0.85	3.2±0.98
平均植株总生物量Average total biomass （T_b）	1.00±0.19	0.97±0.15
平均植株种子数Average seed number （S_n）	395±68.78	425±89.84
平均植株总种子重量Average total seed weight （TS_w）	0.31±0.01	0.35±0.02*
繁殖力Reproduction effort （RE）	31.54±2.72	36.31±1.46*

指标Indicator	RR	SS
分蘖数Tiller number	2.8±0.85	3.2±0.98
平均植株总生物量Average total biomass （T_b）	1.00±0.19	0.97±0.15
平均植株种子数Average seed number （S_n）	395±68.78	425±89.84
平均植株总种子重量Average total seed weight （TS_w）	0.31±0.01	0.35±0.02*
繁殖力Reproduction effort （RE）	31.54±2.72	36.31±1.46*

地点 Location	基因型 Genotype	株高 Plant height （cm）	分蘖数 Tillers number	地上生物量 Aboveground biomass （g·plant^-1）	种子产量 Seed yield （g·plant^-1）
即墨Jimo	RR	60.9±1.82	2.8±0.75	0.42±0.02	0.30±0.02
即墨Jimo	SS	67.2±1.77	3.2±0.93	0.51±0.02*	0.38±0.01*
莱西Laixi	RR	48.9±3.12	2.3±0.33	0.44±0.10	0.32±0.03
莱西Laixi	SS	52.4±2.43	2.6±0.21	0.63±0.07*	0.49±0.06*