The stress regulator FgWhi2 and phosphatase FgPsr1 play crucial roles in the regulation of secondary metabolite biosynthesis and the response to fungicides in Fusarium graminearum

doi:10.1016/j.jia.2024.01.003

Journal of Integrative Agriculture

2025, Vol. 24

Issue (8): 3095-3111 DOI: 10.1016/j.jia.2024.01.003

Plant Protection

Advanced Online Publication | Current Issue | Archive | Adv Search

The stress regulator FgWhi2 and phosphatase FgPsr1 play crucial roles in the regulation of secondary metabolite biosynthesis and the response to fungicides in Fusarium graminearum

Jie Zhang^{1, 2}, Han Gao¹, Fuhao Ren¹, Zehua Zhou³, Huan Wu¹, Huahua Zhao¹, Lu Zhang^{1, 2}, Mingguo Zhou^{1, 2}, Yabing Duan^{1, 2#}

¹ College of Plant Protection, Nanjing Agricultural University, Nanjing 210095, China

² Sanya Institute, Nanjing Agricultural University, Sanya 572025, China

³ Hunan Provincial Key Laboratory for Biology and Control of Plant Pests, Hunan Agricultural University, Changsha 410128, China

Highlights
● FgWhi2 and FgPsr1 are key players in F. graminearum’s responses to osmotic, oxidative, cell membrane, and fungicide stresses.
● FgWhi2 and FgPsr1 are potential targets for developing mycotoxin inhibitors.
● Fluazinam and chlorothalonil inhibit FgWhi2, reducing DON biosynthesis in F. graminearum.

Abstract
References

Download: PDF in ScienceDirect
Export: BibTeX | EndNote (RIS)

摘要

在酵母中，胁迫应答蛋白Whi2与磷酸酶Psr1相互作用并以复合体形式调控生长、繁殖、侵染和胁迫应答，但它们在禾谷镰孢菌中的调控作用尚不明确。为了明确Whi2与Psr1在禾谷镰孢菌中的调控作用，本文鉴定了Whi2和Psr1在禾谷镰孢菌中的同源基因，并通过构建缺失突变体探究其功能。结果表明，FgWHI2与FgPSR1缺失突变体∆Fgwhi2、∆Fgpsr1及双缺失突变体∆Fgwhi2-Fgpsr1对1.2 M NaCl、1.2 M KCl、0.01% H₂O₂、0.05%刚果红及0.05% SDS敏感性显著降低，表明FgWHI2与FgPSR1对禾谷镰孢菌响应外界渗透压胁迫、氧化胁迫、细胞壁胁迫有重要作用。通过对突变体麦角甾醇产量及三唑类药剂敏感性的测定，我们发现FgWHI2与FgPSR1不调控禾谷镰孢菌对三唑类杀菌剂药敏性，但调控禾谷镰孢菌麦角甾醇生物合成。通过对禾谷镰孢菌FgCYP51s基因转录水平的测定，我们发现FgWHI2与FgPSR1正调控FgCYP51-C的转录表达；FgWHI2与FgPSR1过表达能够提高FgCYP51-A的转录水平，但FgWHI2与FgPSR1的缺失对FgCYP51-A的转录水平没有影响；FgWHI2与FgPSR1不调控FgCYP51-B的转录表达。同时，我们发现FgWHI2和FgPSR1参与禾谷镰孢菌的有性生殖和无性生殖。通过研究发现FgWHI2和FgPSR1缺失突变体的脱氧雪腐镰刀烯醇毒素（DON）产量降低超90%，且DON产量与FgWHI2和FgPSR1转录水平呈正相关。此外，我们还观察到FgWHI2和FgPSR1参与调控禾谷镰孢菌对百菌清、氟啶胺、嘧菌酯、氰烯菌酯和寡霉素的敏感性，并发现百菌清与氟啶胺之间存在交互抗性，且百菌清和氟啶胺通过抑制FgWHI2表达来阻碍DON毒素的生物合成。有趣的是，百菌清和氟啶胺处理后，FgWhi2和FgPsr1的亚细胞定位显著改变，并且共定位比例增加。综上所述，这些结果表明FgWHI2和FgPsr1在禾谷镰孢菌胁迫应激反应、生殖过程、次生代谢产物合成和对百菌清和氟啶胺的响应中起着至关重要的作用。通过本文的研究，首次明确了FgWhi2与FgPsr1对禾谷镰孢菌DON毒素生物合成的调控作用，拓展了禾谷镰孢菌DON毒素合成调控网络，为小麦赤霉病防控过程中兼顾“防病”与“降毒”及开发有效的杀菌剂组合提供了潜在靶标、理论依据及技术参考。

Abstract

In yeast, the stress-responsive protein Whi2 interacts with phosphatase Psr1 to form a complex that regulates cell growth, reproduction, infection, and the stress response. However, the roles of Whi2 and Psr1 in Fusarium graminearum remain unclear. In this study, we identified homologous genes of WHI2 and PSR1 in F. graminearum and evaluated their functions by constructing deletion mutants. By comparing the responses of the mutants to different stressors, we found that FgWHI2 and FgPSR1 were involved in responding to osmotic, cell wall and cell membrane stresses, while also affecting the sexual and asexual reproduction in F. graminearum. Our studies demonstrated that FgWHI2 and FgPSR1 regulate the biosynthesis of ergosterol and the transcriptional level of FgCYP51C, which is a CYP51 paralogues unique to Fusarium species. This study also found that the deoxynivalenol (DON) production of FgWHI2 and FgPSR1 deletion mutants was reduced by ≥90% and DON production was positively correlated with the transcriptional levels of FgWHI2 and FgPSR1. In addition, we observed that FgWHI2 and FgPSR1 were involved in regulating the sensitivity of F. graminearum to chlorothalonil, fluazinam, azoxystrobin, phenamacril, and oligomycin. This study revealed cross-resistance between chlorothalonil and fluazinam. Meanwhile, chlorothalonil and fluazinam inhibited DON biosynthesis by altering the normal expression of FgWhi2 and FgPsr1. Interestingly, the subcellular localization of FgWhi2 and FgPsr1 was significantly altered after treatment with chlorothalonil and fluazinam, with increased co-localization. Collectively, these findings indicate that FgWHI2 and FgPSR1 play crucial roles in stress response mechanisms, reproductive processes, secondary metabolite synthesis, and fungicide sensitivity in F. graminearum.

Keywords: DON ergosterol FgWHI2 FgPSR1 fungicides Fusarium graminearum stress responses

Received: 31 July 2023 Online: 05 January 2024 Accepted: 07 November 2023

Fund: This work was supported by the National Key Research and Development Program of China (2022YFD1400100), the Jiangsu Agriculture Science and Technology Innovation Fund, China (CX (21) 2037), the Guidance Foundation of the Hainan Institute of Nanjing Agricultural University, China (NAUSY-MS03) and the Postgraduate Research & Practice Innovation Program of Jiangsu Province, China (KYCX20_0596).

About author: Jie Zhang, E-mail: 2018202061@njau.edu.cn; #Correspondence Yabing Duan, Tel: +86-25-84395641, E-mail: dyb@njau.edu.cn

	Service
	E-mail this article
	Add to citation manager
	E-mail Alert
	RSS
	Articles by authors

Cite this article:

Jie Zhang, Han Gao, Fuhao Ren, Zehua Zhou, Huan Wu, Huahua Zhao, Lu Zhang, Mingguo Zhou, Yabing Duan. 2025. The stress regulator FgWhi2 and phosphatase FgPsr1 play crucial roles in the regulation of secondary metabolite biosynthesis and the response to fungicides in Fusarium graminearum. Journal of Integrative Agriculture, 24(8): 3095-3111.

Barreto J S, Tarouco F M, Godoi F G, Geihs M A, Abreu F E, Fillmann G, Sandrini J Z, Rosa C E. 2018. Induction of oxidative stress by chlorothalonil in the estuarine polychaete Laeonereis acuta. Aquatic Toxicology, 196, 1–8.

Becher R, Weihmann F, Deising H B, Wirsel S G. 2011. Development of a novel multiplex DNA microarray for Fusarium graminearum and analysis of azole fungicide responses. BMC Genomics, 12, 52.

Benitez M S, Hersh M H, Vilgalys R, Clark J S. 2013. Pathogen regulation of plant diversity via effective specialization. Trends in Ecology & Evolution, 12, 705–711.

Bian C H, Duan Y B, Xiu Q, Wang J X, Tao X, Zhou M G. 2021. Mechanism of validamycin A inhibiting DON biosynthesis and synergizing with DMI fungicides against Fusarium graminearum. Molecular Plant Pathology, 22, 769–785.

Boeckstaens M, Llinares E, Van V P, Marini A M. 2014. The TORC1 effector kinase Npr1 fine tunes the inherent activity of the Mep2 ammonium transport protein. Nature Communications, 5, 3101.

Buied A, Moore C B, Denning D W, Bowyer P. 2012. High-level expression of cyp51B in azole-resistant clinical Aspergillus fumigatus isolates. The Journal of Antimicrobial Chemotherapy, 68, 512–514.

Cai E P, Li L Y, Deng Y Z, Sun S Q, Jia H, Wu R R, Zhang L H, Jiang Z D, Chang C Q. 2021. MAP kinase Hog1 mediates a cytochrome P450 oxidoreductase to promote the Sporisorium scitamineum cell survival under oxidative stress. Environmental Microbiology, 23, 3306–3317.

Cai S Y, Liu T T, Zhang Y, Wan J, Yang S, Zhao J, Yang J Y. 2012. Homology modeling of different CYP51 subtypes from Magnaporthe grisea and comparison of their binding models with diniconazole. Chemistry & Bioengineering, 29, 17–21. (in Chinese)

Chen X, Wang G, Zhang Y, Margaret D B, Diny N L, Zhao M, Ge H, Sing C N, Metz K A, Stolp Z D. 2018. Whi2 is a conserved negative regulator of TORC1 in response to low amino acids. PLoS Genetics, 14, e1007592.

Cheng J, Riaz M, Yan L, Zeng Z J, Jiang C C. 2022. Increasing media pH contribute to the absorption of boron via roots to promote the growth of citrus. Plant Physiology and Biochemistry, 178, 116–124.

Chung K R. 2012. Stress response and pathogenicity of the necrotrophic fungal pathogen Alternaria Alternata Scientifica, 2012, 635431.

Desjardins A E. 2006. Fusarium Mycotoxins: Chemistry Genetics and Biology. American Phytopathological Society, St. Paul. MN, USA. p. 268.

Ding X F, Luo C, Ren K Q, Zhang J, Zhou J L, Hu X, Liu R S, Wang Y, Gao X, Zhang J. 2008. Characterization and expression of a human KCTD1 gene containing the BTB domain, which mediates transcriptional repression and homomeric interactions. DNA & Cell Biology, 27, 257–265.

Duan Y B, Lu F, Zhou Z H, Zhao H H, Zhang J, Mao Y S, Li M X, Wang J X, Zhou M G. 2020. Quinone outside inhibitors affect DON biosynthesis, mitochondrial structure and toxisome formation in Fusarium graminearum. Journal of Hazardous Materials, 398, 122908.

Duan Y B, Xiao X M, Li T, Chen W W, Wang, J X, Fraaije B A, Zhou M G. 2018. Impact of epoxiconazole on Fusarium head blight control, grain yield and deoxynivalenol accumulation in wheat. Pesticide Biochemistry and Physiology, 152, 138–147.

Ellsworth M, Ostrosky Z L. 2020. Isavuconazole: Mechanism of action, clinical efficacy, and resistance. Journal of Fungi, 6, 324–333.

Fan J R, Urban M, Parker J E, Brewer H C, Kelly S L, Hammond K K, Fraaije B A, Liu X L, Cools H J. 2013. Characterization of the sterol 14 alpha-demethylases of Fusarium graminearum identifies a novel genus-specific CYP51 function. New Phytologist, 198, 821–835.

Fraczek M G, Bromley M, Bowyer P. 2011. An improved model of the Aspergillus fumigatus CYP51A protein. Antimicrobial Agents and Chemotherapy, 55, 2483–2486.

Goswami R S, Kistler H C. 2004. Heading for disaster: Fusarium graminearum on cereal crops. Molecular Plant Pathology, 5, 515–525.

Gu Q, Zhang C Q, Yu F W, Yin Y N, Shim W B, Ma Z H. 2015. Protein kinase FgSch9 serves as a mediator of the target of rapamycin and high osmolarity glycerol pathways and regulates multiple stress responses and secondary metabolism in Fusarium graminearum. Environmental Microbiology, 17, 2661–2676.

Harata K, Nishiuchi T, Kubo Y. 2016. Colletotrichum orbiculare Whi2, a Yeast Stress-response regulator homology, controls the biotrophic stage of hemibiotrophic infection through TOR signaling. Molecular Plant Microbe Interactions, 29, 468–483.

Hohmann S. 2002. Osmotic stress signaling and osmoadaptation in yeasts. Microbiology and Molecular Biology Reviews, 66, 300–372.

Hua J, Jones D K, Mattes B M, Cothran R D, Relyea R A, Hoverman J T. 2015. Evolved pesticide tolerance in amphibians: Predicting mechanisms based on pesticide novelty and mode of action. Environmental Pollution, 206, 56–63.

Jiang J H, Yun Y Z, Yang Q Q, Shim W B, Wang Z, Ma Z H. 2011. A type 2C protein phosphatase FgPtc3 is involved in cell wall integrity, lipid metabolism, and virulence in Fusarium graminearum. PLoS ONE, 6, e25311.

Leadsham J E, Miller K, Ayscough K R, Colombo S, Martegani E, Sudbery P, Gourlay C W. 2009. Whi2p links nutritional sensing to actin-dependent Ras-cAMP-PKA regulation and apoptosis in yeast. Journal of Cell Science, 122, 706–715.

Liu S M, Duan Y B, Ge C Y, Chen C J, Zhou M G. 2013. Functional analysis of the β2-tubulin gene of Fusarium graminearum and the β-tubulin gene of Botrytis cinerea by homologous replacement. Pest Management Science, 69, 582–588.

Liu X, Jiang J H, Yin Y N, Ma Z H. 2012. Involvement of FgERG4 in ergosterol biosynthesis, vegetative differentiation and virulence in Fusarium graminearum. Molecular Plant Pathology, 14, 71–83.

Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C (T)) Method. Methods, 25, 402–408.

Martel C M, Parker J E, Warrilow A, Rolley N J, Kelly S L, Kelly D E. 2010. Complementation of a ERG11/CYP51 (Sterol 14α-Demethylase) doxycycline-regulated mutant and screening of the azole sensitivity of isoenzymes CYP51A and CYP51B. Antimicrobial Agents and Chemotherapy, 54, 4920–4923.

Mascaraque V, Hernaez M L, Jimenez S M, Hansen R, Gil C, Martin H, Molina M. 2012. Phosphoproteomic analysis of protein kinase C signaling in Saccharomyces cerevisiae reveals Slt2 MAPK-dependent phosphorylation of eisosome core components. Molecular & Cellular Proteomics, 12, 557–574.

McCormick S P, Stanley A M, Stover N A, Alexander N J. 2011. Trichothecenes: From simple to complex mycotoxins. Toxins, 3, 802–814.

Meng S, Qiu J H, Xiong M, Liu Z Q, Jane S J, Lin F H, Shi H B, Kou Y J. 2021. UvWhi2 is required for stress response and pathogenicity in Ustilaginoidea virens. Rice Science, 29, 47–54.

Nguyen T H, Chang H L. 2020. Roles of farnesyl-diphosphate farnesyltransferase 1 in tumour and tumour microenvironments. Cells, 9, 2352–2384.

Olsson P A, Larsson L, Bago B, Wallander H, Van Aarle I M. 2003. Ergosterol and fatty acids for biomass estimation of mycorrhizal fungi. New Phytologist, 159, 7–10.

Osborne L E, Stein J M. 2007. Epidemiology of Fusarium head blight on small-grain cereals. Interantional Journal of Food Microbiology, 119, 103–108.

Pearson M M, Rogers P D, Cleary J D, Chapman S W. 2003. Voriconazole: A new triazole antifungal agent. Annals of Pharmacotherapy, 37, 420–432.

Peffer R C, Moggs J G, Timothy P, Currie R A, Wright J, Milburn G, Waechter F, Rusyn I. 2007. Mouse liver effects of cyproconazole, a triazole fungicide: Role of the constitutive androstane receptor. Toxicological Sciences, 99, 315–325.

Philip C. 2000. The regulation of protein function by multisite phosphorylation - A 25 years update. Trends in Biochemical Sciences, 25, 596–601.

Quinn J. 2008. Chapter 5 Differences in stress responses between model and pathogenic fungi. Elsevier Science & Technology, 27, 67–85.

Roundtree M T, Juvvadi P R, Shwab E K, Cole D C, Steinbach W J. 2020. Aspergillus fumigatus Cyp51A and Cyp51B proteins are compensatory in function and localize differentially in response to antifungals and cell wall inhibitors. Antimicrobial Agents and Chemotherapy, 64, e00735–20.

Shi H B, Meng S, Qiu J H, Wang C C, Shu Y Z, Luo C X, Kou Y J. 2021. MoWhi2 regulates appressorium formation and pathogenicity via the MoTor signalling pathway in Magnaporthe oryzae. Molecular Plant Pathology, 22, 969–983.

Son H, Seo Y S, Min K, Park A R, Lee J, Jin J M, Lin Y, Cao P, Hong S Y, Kim E K, Lee S H, Cho A, Lee S, Kim M G, Kim Y, Kim J E, Kim J C, Choi G J, Yun S H, Lim J Y, et al. 2011. A phenome-based functional analysis of transcription factors in the cereal head blight fungus, Fusarium graminearum. PLoS Pathogens, 7, e1002310.

Sudbery P E, Goodey A R, Carter B L. 1980. Genes which control cell proliferation in the yeast Saccharomyces cerevisiae. Nature, 288, 401–404.

Suzuki K, Sugimoto K, Hayashi H, Komyoji T. 2009. Biological mode of action of fluazinam, a new fungicide, for Chinese cabbage clubroot. Japanese Journal of Phytopathology, 61, 395–398.

Tate J J, Marsikova J, Vachova L, Palkova Z, Cooper T G. 2021. Effects of abolishing Whi2 on the proteome and nitrogen catabolite repression-sensitive protein production. G3 - Genes Genomes Genetics, 12, jkab432.

Teige M, Scheikl E, Eulgem T, Hirt H. 2004. The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Molecular Cell, 15, 141–152.

Teng X C, Hardwick J M. 2019. Whi2: A new player in amino acid sensing. Current Genetics, 65, 701–709.

Timpano H, Tong L C, Gautier V, Lalucque H, Silar P. 2016. The PaPsr1 and PaWhi2 genes are members of the regulatory network that connect stationary phase to mycelium differentiation and reproduction in Podospora anserina. Fungal Genetics & Biology, 94, 1–10.

Xiong M, Meng S, Qiu J H, Shi H B, Shen X L, Kou Y J. 2020. Putative phosphatase UvPsr1 is required for mycelial growth, conidiation, stress response and pathogenicity in Ustilaginoidea virens. Rice Science, 27, 529–536.

Xu C, Li M X, Zhou Z H, Li J, Chen D M, Duan Y B, Zhou M G. 2019. Impact of five succinate dehydrogenase inhibitors on DON biosynthesis of Fusarium asiaticum, causing Fusarium head blight in wheat. Toxins, 11, 272–288.

Yan X, Ma W B, Li Y, Wang H, Que Y W, Ma Z H, Talbot N J, Wang Z Y. 2011. A sterol 14a-demethylase is required for conidiation, virulence and for mediating sensitivity to sterol demethylation inhibitors by the rice blast fungus Magnaporthe oryzae. Fungal Genetics and Biology, 48, 144–153.

Yin W B, Zhang Y X, Cui H X, Jiang H, Liu L, Zheng Y, Wu T X, Zhao L Y, Sun Y, Su X, Li S, Zhao D M, Cheng M S. 2021. Design, synthesis and evaluation of novel 5-phenylthiophene derivatives as potent fungicidal of Candida albicans and antifungal reagents of fluconazole-resistant fungi. European Journal of Medicinal Chemistry, 225, 113740–113754.

Yun Y Z, Liu Z Y, Yin Y N, Jiang J H, Chen Y, Xu J R, Ma Z H. 2015. Functional analysis of the Fusarium graminearum phosphatome. New Phytologist, 207, 119–134.

Yun Y Z, Liu Z Y, Zhang J Z, Shim W B, Chen Y, Ma Z H. 2013. The MAPKK FgMkk1 of Fusarium graminearum regulates vegetative differentiation, multiple stress response, and virulence via the cell wall integrity and high-osmolarity glycerol signaling pathways. Environmental Microbiology, 16, 2023–2037.

Zhao H H, Tao X, Song W, Xu H R, Li M X, Cai Y Q, Wang J X, Duan Y B. 2022. Mechanism of Fusarium graminearum resistance to ergosterol biosynthesis inhibitors: G443S substitution of the drug target FgCYP51A. Journal of Agricultural and Food Chemistry, 70, 1788–1798.

Zheng K, Pinglay S, Ji H K, Boeke J D. 2017. Msn2/4 regulate expression of glycolytic enzymes and control transition from quiescence to growth. eLife, 6, e29938.

Zhou Z H, Duan Y B, Zhou M G. 2020. Carbendazim-resistance associated β2-tubulin substitutions increase deoxynivalenol biosynthesis by reducing the interaction between β2-tubulin and IDH3 in Fusarium graminearum. Environmental Microbiology, 22, 598–614.

[1]	Haiyang Li, Yuan Zhang, Cancan Qin, Zhifang Wang, Lingjun Hao, Panpan Zhang, Yongqiang Yuan, Chaopu Ding, Mengxuan Wang, Feifei Zan, Jiaxing Meng, Xunyu Zhuang, Zheran Liu, Limin Wang, Haifeng Zhou, Linlin Chen, Min Wang, Xiaoping Xing, Hongxia Yuan, Honglian Li, Shengli Ding. Identification and characterization of FpRco1 in regulating vegetative growth and pathogenicity based on T-DNA insertion in Fusarium pseudograminearum[J]. >Journal of Integrative Agriculture, 2024, 23(9): 3055-3065.
[2]	Jia Chen, Xinran Zhang, Ziqi He, Dongwei Xiong, Miao Long. Damage on intestinal barrier function and microbial detoxification of deoxynivalenol: A review[J]. >Journal of Integrative Agriculture, 2024, 23(8): 2507-2524.
[3]	Jiawei Pan, Jia Song, Rahat Sharif, Xuewen Xu, Shutong Li, Xuehao Chen. A mutation in the promoter of the yellow stripe-like transporter gene in cucumber results in a yellow cotyledon phenotype [J]. >Journal of Integrative Agriculture, 2024, 23(3): 849-862.
[4]	SUN Yan, LI Yu-hua, ZHAO Chang-heng, TENG Jun, WANG Yong-hui , WANG Tian-qi, SHI Xiao-yuan, LIU Zi-wen, LI Hai-jing, WANG Ji-jing, WANG Wen-wen, NING Chao, WANG Chang-fa, ZHANG Qin. Genome-wide association study for numbers of vertebrae in Dezhou donkey population reveals new candidate genes[J]. >Journal of Integrative Agriculture, 2023, 22(10): 3159-3169.
[5]	ZHANG Hui-min, JIANG Hong-rui, CHEN Dai-jie, SHEN Zi-liang, MAO Yong-jiang, LIANG Yu-sheng, Juan J. LOOR, YANG Zhang-ping. Evaluation of a povidone-iodine and chitosan-based barrier teat dip in the prevention of mastitis in dairy cows[J]. >Journal of Integrative Agriculture, 2021, 20(6): 1615-1625.
[6]	ZHANG Shu-juan, LI Yu-lian, SONG Guo-qi, GAO Jie, ZHANG Rong-zhi, LI Wei, CHEN Ming-li, LI Gen-ying. *Heterologous expression of the ThIPK2* gene enhances drought resistance of common wheat**[J]. >Journal of Integrative Agriculture, 2020, 19(4): 941-952.
[7]	WANG Qian-nan, HUANG Pan-pan, ZHOU Shan-yue. Functional characterization of the catalytic and bromodomain of FgGCN5 in development, DON production and virulence of Fusarium graminearum[J]. >Journal of Integrative Agriculture, 2020, 19(10): 2477-2487.
[8]	Sophiarani Yengkhom, Arif Uddin, Supriyo Chakraborty. Deciphering codon usage patterns and evolutionary forces in chloroplast genes of Camellia sinensis var. assamica and Camellia sinensis var. sinensis in comparison to Camellia pubicosta[J]. >Journal of Integrative Agriculture, 2019, 18(12): 2771-2785.
[9]	SONG Hui, LIU Jing, CHEN Tao, NAN Zhi-biao. Synonymous codon usage pattern in model legume Medicago truncatula[J]. >Journal of Integrative Agriculture, 2018, 17(09): 2074-2081.
[10]	WU Yan-qing, LI Zhi-yuan, ZHAO Da-qiu, TAO Jun. *Comparative analysis of flower-meristem-identity gene APETALA2* (AP2) codon in different plant species**[J]. >Journal of Integrative Agriculture, 2018, 17(04): 867-877.
[11]	YAN Song, ZHU Shan, MAO Ling-hua, HUANG Ren-liang, XIONG Hong-liang, SHEN Lin-jun, SHEN. *Molecular identification of the cytoplasmic male sterile source from Dongxiang wild rice (Oryza rufipogon* Griff.)**[J]. >Journal of Integrative Agriculture, 2017, 16(08): 1669-1675.
[12]	YANG Cui, XU Yu, JIA Ren-yong, LIU Si-yang, WANG Ming-shu, ZHU De-kang, CHEN Shun, LIU Ma-feng, ZHAO Xin-xin, SUN Kun-feng, JING Bo, YIN Zhong-qiong, CHENG An-chun . The codon-optimized capsid gene of duck circovirus can be highly expressed in yeast and self-assemble into virus-like particles[J]. >Journal of Integrative Agriculture, 2017, 16(07): 1601-1608.
[13]	Christopher Brown, Antony P. Martin, Christopher P. L. Grof. *The application of Fourier transform mid-infrared (FTIR) spectroscopy to identify variation in cell wall composition of Setaria italica* ecotypes**[J]. >Journal of Integrative Agriculture, 2017, 16(06): 1256-1267.
[14]	HE Liang-qiong1, TANG Rong-hua1, JIANG Jing1, XIONG Fa-qian1, HUANG Zhi-peng1, WU Hai-ning1, GAO Zhong-kui1, ZHONG Rui-chun1, HE Xin-hua2, HAN Zhu-qiang1 . *Rapid gene expression change in a novel synthesized allopolyploid population of cultivated peanut×Arachis doigoi* cross by cDNA-SCoT and HFO-TAG technique**[J]. >Journal of Integrative Agriculture, 2017, 16(05): 1093-1102.
[15]	LIU Dong-hua, HAN Hao-yuan, ZHANG Xin, SUN Ting, LAN Xian-yong, CHEN Hong, LEI Chu-zhao, DANG Rui-hua . *The genetic diversity analysis in the donkey myostatin* gene**[J]. >Journal of Integrative Agriculture, 2017, 16(03): 656-663.

No Suggested Reading articles found!

Viewed

Full text

Abstract

Cited

Shared

Discussed

Cite this article:

About JIA

Editorial board

For authors