In-Depth Understanding of the Genetic Control of Stripe Rust Resistance (Puccinia striiformis f. sp. tritici) Induced in Wheat (Triticum aestivum) by Trichoderma asperellum T34
- Samar M. Esmail1
- Ghady E. Omar1
- Amira M. I. Mourad2 3 †
- 1Wheat Disease Research Department, Plant Pathology Research Institute, Agricultural Research Center, Giza, Egypt
- 2Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Germany
- 3Department of Agronomy, Faculty of Agriculture, Assiut University, Assiut, Egypt
Abstract
Wheat stripe rust (caused by Puccinia striiformis f. tritici Erikss.) causes severe yield losses worldwide. Due to the continuous appearance of new stripe rust races, resistance has been broken in most of the highly resistant genotypes in Egypt and worldwide. Therefore, looking for new ways to resist such a severe disease is urgently needed. Trichoderma asperellum strain T34 has been known as an effective bioagent against many crop diseases. It exists naturally in Egyptian fields. Therefore, in our study, the effectiveness of strain T34 was tested as a bioagent against wheat stripe rust. For this purpose, 198 spring wheat genotypes were tested for their resistance against two different P. striiformis f. tritici populations collected from the Egyptian fields. The most highly aggressive P. striiformis f. tritici population was used to test the effectiveness of strain T34. Highly significant differences were found between strain T34 and stripe rust, suggesting the effectiveness of strain T34 in stripe rust resistance. A genome-wide association study identified 48 gene models controlling resistance under normal conditions and 46 gene models controlling strain T34-induced resistance. Of these gene models, only one common gene model was found, suggesting the presence of two different genetic systems controlling resistance under each condition. The pathways of the biological processes were investigated under both conditions. This study provided in-depth understanding of genetic control and, hence, will accelerate the future of wheat breeding programs for stripe rust resistance.
Literature Cited
- 2022. Identification of putative SNP markers associated with resistance to Egyptian loose smut race(s) in spring barley. Genes (Basel) 13:1075. https://doi.org/10.3390/genes13061075 Crossref, ISI, Google Scholar
- 2021. Genomic regions associated with stripe rust resistance against the Egyptian race revealed by genome-wide association study. BMC Plant Biol. 21:42. https://doi.org/10.1186/s12870-020-02813-6 Crossref, ISI, Google Scholar
- 2021. Genetic diversity, linkage disequilibrium and population structure of Bulgarian bread wheat assessed by genome-wide distributed SNP markers: From old germplasm to semi-dwarf cultivars. Plants (Basel) 10:1116. https://doi.org/10.3390/plants10061116 Crossref, Google Scholar
- 2020. GWAS: Fast-forwarding gene identification and characterization in temperate cereals: Lessons from barley—A review. J. Adv. Res. 22:119‐135. https://doi.org/10.1016/j.jare.2019.10.013 Crossref, ISI, Google Scholar
- 2016. Genome analysis and avirulence gene cloning using a high-density RADseq linkage map of the flax rust fungus, Melampsora lini. BMC Genomics 17:667. https://doi.org/10.1186/s12864-016-3011-9 Crossref, ISI, Google Scholar
- 2019. The plant hypersensitive response: Concepts, control and consequences. Mol. Plant Pathol. 20:1163‐1178. https://doi.org/10.1111/mpp.12821 Crossref, ISI, Google Scholar
- 2009. Role of plant hormones in plant defence responses. Plant Mol. Biol. 69:473‐488. https://doi.org/10.1007/s11103-008-9435-0 Crossref, ISI, Google Scholar
- 2018. The status of biological control and recommendations for improving uptake for the future. BioControl 63:155‐167. https://doi.org/10.1007/s10526-017-9831-y Crossref, ISI, Google Scholar
- 2020. Molecular characterization of the purine degradation pathway genes ALA1 and URE1 of the maize anthracnose fungus Colletotrichum graminicola identified urease as a novel target for plant disease control. Phytopathology 110:1530‐1540. https://doi.org/10.1094/PHYTO-04-20-0114-R Link, ISI, Google Scholar
- 2021. Globally important wheat diseases: Status, challenges, breeding and genomic tools to enhance resistance durability. Pages 59‐128 in: Genomic Designing for Biotic Stress Resistant Cereal Crops. C. Kole, ed. Springer, New Delhi, India. Google Scholar
- 2021. Trichoderma longibrachiatum (TG1) enhances wheat seedlings tolerance to salt stress and resistance to Fusarium pseudograminearum. Front. Plant Sci. 12:741231. https://doi.org/10.3389/fpls.2021.741231 Crossref, ISI, Google Scholar
- 2012. Effect of ammonium/nitrate ratio in nutrient solution on control of Fusarium wilt of tomato by Trichoderma asperellum T34. Plant Pathol. 61:132‐139. https://doi.org/10.1111/j.1365-3059.2011.02490.x Crossref, ISI, Google Scholar
- 2007. TASSEL: Software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633‐2635. https://doi.org/10.1093/bioinformatics/btm308 Crossref, ISI, Google Scholar
- 2018. Trends in biological control: Public interest, international networking and research direction. BioControl 63:11‐26. https://doi.org/10.1007/s10526-017-9850-8 Crossref, ISI, Google Scholar
- 1971. Pathogenic specialization in cereal rust fungi, especially Puccinia recondita f. sp. tritici: Concepts, methods of study and application. Tech. Bull. No. 1432. United States Department of Agriculture, Economic Research Service. https://doi.org/10.22004/ag.econ.171860 Google Scholar
- 2007. Salicylic acid in plant disease resistance. Pages 335‐370 in: Salicylic Acid: A Plant Hormone. S. Hayat, and A. Ahmad, eds. Springer, Dordrecht, The Netherlands. https://doi.org/10.1007/1-4020-5184-0_12 Google Scholar
- 2005. Epidemiology and control of stripe rust [Puccinia striiformis f. sp. tritici] on wheat. Can. J. Plant Pathol. 27:314‐337. https://doi.org/10.1080/07060660509507230 Crossref, ISI, Google Scholar
- 2011. Programmed cell death in the plant immune system. Cell Death Differ. 18:1247‐1256. https://doi.org/10.1038/cdd.2011.37 Crossref, ISI, Google Scholar
- 2019. Transcriptome and metabolome reprogramming in tomato plants by Trichoderma harzianum strain T22 primes and enhances defense responses against aphids. Front. Physiol. 10:745. https://doi.org/10.3389/fphys.2019.00745 Crossref, ISI, Google Scholar
- 2007. Trichoderma spp. as elicitors of wheat plant defense responses against Septoria tritici. Biocontrol Sci. Technol. 17:687‐698. https://doi.org/10.1080/09583150701527094 Crossref, ISI, Google Scholar
- 2022. Ensembl 2022. Nucleic Acids Res. 50:D988‐D995. https://doi.org/10.1093/nar/gkab1049 Crossref, ISI, Google Scholar .
- 2020. Biological management of banana Fusarium wilt caused by Fusarium oxysporum f. sp. cubense tropical race 4 using antagonistic fungal isolate CSR-T-3 (Trichoderma reesei). Front. Microbiol. 11:595845. https://doi.org/10.3389/fmicb.2020.595845 Crossref, ISI, Google Scholar
- 2019. A comparison of mainstream genotyping platforms for the evaluation and use of barley genetic resources. Front. Plant Sci. 10:544. https://doi.org/10.3389/fpls.2019.00544 Crossref, ISI, Google Scholar
- 2007. Anion channels and transporters in plant cell membranes. FEBS Lett. 581:2367‐2374. https://doi.org/10.1016/j.febslet.2007.04.003 Crossref, ISI, Google Scholar
- 2017. How does the multifaceted plant hormone salicylic acid combat disease in plants and are similar mechanisms utilized in humans? BMC Biol. 15:23. https://doi.org/10.1186/s12915-017-0364-8 Crossref, ISI, Google Scholar
- 2022. Direct inhibition of phosphate transport by immune signaling in Arabidopsis. Curr. Biol. 32:488‐495.e5. https://doi.org/10.1016/j.cub.2021.11.063 Crossref, ISI, Google Scholar
- 2019. Changeability in stripe rust infection and grainy yield of wheat associated to climatic conditions. Environ. Biodiversity Soil Secur. 2:143‐153. https://doi.org/10.21608/JENVBS.2019.6674.1040 Google Scholar
- 2016. Protein phosphatase 2A in the regulatory network underlying biotic stress resistance in plants. Front. Plant Sci. 7:812. https://doi.org/10.3389/fpls.2016.00812 Crossref, ISI, Google Scholar
- 2019. Evaluation of a global spring wheat panel for stripe rust: Resistance loci validation and novel resources identification. PLoS One 14:e0222755. https://doi.org/10.1371/journal.pone.0222755 Crossref, ISI, Google Scholar
- 2018. A comparison between genotyping-by-sequencing and array-based scoring of SNPs for genomic prediction accuracy in winter wheat. Plant Sci. 270:123‐130. https://doi.org/10.1016/j.plantsci.2018.02.019 Crossref, ISI, Google Scholar
- 2020. Suppression of wheat strip rust disease caused by Puccinia striiformis f. sp. tritici by eco-friendly bio-control agents correlated with yield improvement. Fresenius Environ. Bull. 29:8385‐8393. ISI, Google Scholar
- 2018. Biocontrol of stem rust disease of wheat using arbuscular mycorrhizal fungi and Trichoderma spp.. Physiol. Mol. Plant Pathol. 103:84‐91. https://doi.org/10.1016/j.pmpp.2018.05.002 Crossref, ISI, Google Scholar
- 2022. Genome-wide association mapping revealed SNP alleles associated with spike traits in wheat. Agronomy 12:1469. https://doi.org/10.3390/agronomy12061469 Crossref, Google Scholar
- 2021. GWAS revealed effect of genotypes × environment interactions for grain yield of Nebraska winter wheat. BMC Genomics 22:2. https://doi.org/10.1186/s12864-020-07308-0 Crossref, ISI, Google Scholar
EPA . 2011. Trichoderma asperellum strain T34 (119209) fact sheet. United States Environmental Protection Agency. https://www3.epa.gov/pesticides/chem_search/reg_actions/registration/fs_PC-119209_01-Oct-11.pdf Google Scholar- 2021. Emergence of new aggressive races of Puccinia striiformis f. sp. tritici causing yellow rust epiphytotic in Egypt. Physiol. Mol. Plant Pathol. 114:101612. https://doi.org/10.1016/j.pmpp.2021.101612 Crossref, ISI, Google Scholar
- 2014. Increased rhizosphere populations of Trichoderma asperellum strain T34 caused by secretion pattern of root exudates in tomato plants inoculated with Botrytis cinerea. Biol. Control 78:77‐85. Crossref, ISI, Google Scholar
- 2014. Functional characterization of a Nudix hydrolase AtNUDX8 upon pathogen attack indicates a positive role in plant immune responses. PLoS One 9:e114119. https://doi.org/10.1371/journal.pone.0114119 Crossref, ISI, Google Scholar
- 2012. Identification of indole-3-carboxylic acid as mediator of priming against Plectosphaerella cucumerina. Plant Physiol. Biochem. 61:169‐179. https://doi.org/10.1016/j.plaphy.2012.10.004 Crossref, ISI, Google Scholar
- 2006. Early signaling events induced by elicitors of plant defenses. Mol. Plant-Microbe Interact. 19:711‐724. https://doi.org/10.1094/MPMI-19-0711 Link, ISI, Google Scholar
- 2013. Strategies for wheat stripe rust pathogenicity identified by transcriptome sequencing. PLoS One 8:e67150. https://doi.org/10.1371/journal.pone.0067150 Crossref, ISI, Google Scholar
- 2020. ShinyGO: A graphical gene-set enrichment tool for animals and plants. Bioinformatics 36:2628‐2629. https://doi.org/10.1093/bioinformatics/btz931 Crossref, ISI, Google Scholar
- 2017. Sugar accumulation in leaves of Arabidopsis sweet11/sweet12 double mutants enhances priming of the salicylic acid-mediated defense response. Front. Plant Sci. 8:1378. https://doi.org/10.3389/fpls.2017.01378 Crossref, ISI, Google Scholar
- 2016. De novo centromere formation and centromeric sequence expansion in wheat and its wide hybrids. PLoS Genet. 12:e1005997. https://doi.org/10.1371/journal.pgen.1005997 Crossref, ISI, Google Scholar
- 2019. Management of barley net blotch using Trichoderma asperellum (T34), eugenol, non-traditional compounds and fungicides. Egypt J. Biol. Pest Control 29:88. https://doi.org/10.1186/s41938-019-0179-8 Crossref, ISI, Google Scholar
- 2018. Biological control of Podosphaera xanthii the causal agent of squash powdery mildew disease by upregulation of defense-related enzymes. Egypt. J. Biol. Pest Control 28:57. https://doi.org/10.1186/s41938-018-0058-8 Crossref, ISI, Google Scholar
- 2021. KnetMiner: A comprehensive approach for supporting evidence-based gene discovery and complex trait analysis across species. Plant Biotechnol. J. 19:1670‐1678. https://doi.org/10.1111/pbi.13583 Crossref, ISI, Google Scholar
- 2022. High-LD SNP markers exhibiting pleiotropic effects on salt tolerance at germination and seedlings stages in spring wheat. Plant Mol. Biol. 108:585‐603. https://doi.org/10.1007/s11103-022-01248-x Crossref, ISI, Google Scholar
- 2016. Major gene for field stem rust resistance co-locates with resistance gene sr12 in “Thatcher” wheat. PLoS One 11:e0157029. https://doi.org/10.1371/journal.pone.0157029 Crossref, ISI, Google Scholar
- 2018. An efficient approach for the development of genome-specific markers in allohexaploid wheat (Triticum aestivum L.) and its application in the construction of high-density linkage maps of the D genome. DNA Res. 25:317‐326. https://doi.org/10.1093/dnares/dsy004 Crossref, ISI, Google Scholar
- 1997. Elicitor-stimulated ion fluxes and O2− from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley. Proc. Natl. Acad. Sci. U.S.A. 94:4800‐4805. https://doi.org/10.1073/pnas.94.9.4800 Crossref, ISI, Google Scholar
- 2016. Effect of methyl salicylate (MeSA), an elicitor on growth, physiology and pathology of resistant and susceptible rice varieties. Sci. Rep. 6:34498. https://doi.org/10.1038/srep34498 Crossref, ISI, Google Scholar
- 2020. Comparing different statistical models and multiple testing corrections for association mapping in soybean and maize. Front. Plant Sci. 10:1794. https://doi.org/10.3389/fpls.2019.01794 Crossref, ISI, Google Scholar
- 1967. Reproductive potentials of races 15B and 56 of wheat stem rust. Can. J. Bot. 45:1077‐1091. https://doi.org/10.1139/b67-113 Crossref, Google Scholar
- 2012. SNP discovery through next-generation sequencing and its applications. Int. J. Plant Genomics 2012:831460. https://doi.org/10.1155/2012/831460 Crossref, Google Scholar
- 2014. Lr1-mediated leaf rust resistance pathways of transgenic wheat lines revealed by a gene expression study using the Affymetrix GeneChip® Wheat Genome Array. Mol. Breed. 34:127‐141. https://doi.org/10.1007/s11032-014-0022-6 Crossref, ISI, Google Scholar
- 2020. Trichoderma counteracts the challenge of Phytophthora nicotianae infections on tomato by modulating plant defense mechanisms and the expression of crinkler, necrosis-inducing Phytophthora protein 1, and cellulose-binding elicitor lectin pathogenic effectors. Front. Plant Sci. 11:583539. https://doi.org/10.3389/fpls.2020.583539 Crossref, ISI, Google Scholar
- 2014. Modulation of RNA polymerase II phosphorylation downstream of pathogen perception orchestrates plant immunity. Cell Host Microbe 16:748‐758. https://doi.org/10.1016/j.chom.2014.10.018 Crossref, ISI, Google Scholar
- 2020. Comparative transcriptome analysis reveals key pathways and hub genes in rapeseed during the early stage of Plasmodiophora brassicae infection. Front. Genet. 10:1275. https://doi.org/10.3389/fgene.2019.01275 Crossref, ISI, Google Scholar
- 2016. Iterative usage of fixed and random effect models for powerful and efficient genome-wide association studies. PLoS Genet. 12:e1005767. https://doi.org/10.1371/journal.pgen.1005767 Crossref, ISI, Google Scholar
- 2016. Molecular characterization and antagonistic potential of phenazine-1-carboxylic acid producing Pseudomonas fluorescens isolates from economically important crops in South India. Int. J. Clin. Biol. Sci. 1:30. Google Scholar
- 2016. Compost from forest cleaning green waste and Trichoderma asperellum strain T34 reduced incidence of Fusarium circinatum in Pinus radiata seedlings. Biol. Control 95:31‐39. https://doi.org/10.1016/j.biocontrol.2015.12.014 Crossref, ISI, Google Scholar
- 2015. Neuropeptide receptors npr-1 and npr-2 regulate Caenorhabditis elegans avoidance response to the plant stress hormone methyl salicylate. Genetics 199:523‐531. https://doi.org/10.1534/genetics.114.172239 Crossref, ISI, Google Scholar
- 2012. Salicylic acid regulates basal resistance to Fusarium head blight in wheat. Mol. Plant-Microbe Interact. 25:431‐439. https://doi.org/10.1094/MPMI-09-11-0232 Link, ISI, Google Scholar
- 2018. The defense-related isoleucic acid differentially accumulates in Arabidopsis among branched-chain amino acid-related 2-hydroxy carboxylic acids. Front. Plant Sci. 9:766. https://doi.org/10.3389/fpls.2018.00766 Crossref, ISI, Google Scholar
- 2008. Emergence of a novel population of Puccinia striiformis f. sp. tritici in eastern United States. Phytopathology 98:632‐639. https://doi.org/10.1094/PHYTO-98-6-0632 Link, ISI, Google Scholar
- 1971. A uniform system for recording and processing cereal research data. United States Department of Agriculture–Agricultural Research Service. https://books.google.com.eg/books/about/A_uniform_system_for_recording_and_proce.html?id=XN7NYgEACAAJ&redir_esc=y Google Scholar
- 2018. Current challenges to the implementation of classical biological control. BioControl 63:1-9. https://doi.org/10.1007/s10526-017-9862-4 Crossref, ISI, Google Scholar
- 2011. Transcription dynamics in plant immunity. Plant Cell 23:2809‐2820. https://doi.org/10.1105/tpc.111.087346 Crossref, ISI, Google Scholar
- 2021. Trichoderma and the plant heritable priming responses. J. Fungi 7:318. https://doi.org/10.3390/jof7040318 Crossref, ISI, Google Scholar
- 2021. Identification of candidate genes and genomic regions associated with adult plant resistance to stripe rust in spring wheat. Agronomy 11:2585. https://doi.org/10.3390/agronomy11122585 Crossref, Google Scholar
- 2019a. Recent advances in wheat (Triticum spp.) breeding. Pages 559-593 in: Advances in Plant Breeding Strategies: Cereals. J.Al-Khayri, S.Jain, and D.Johnson, eds. Springer, Cham, Switzerland. https://doi.org/10.1007/978-3-030-23108-8_15 Crossref, Google Scholar
- 2020. Molecular genetic analysis of spring wheat core collection using genetic diversity, population structure, and linkage disequilibrium. BMC Genomics 21:434. https://doi.org/10.1186/s12864-020-06835-0 Crossref, ISI, Google Scholar
- 2022. Genome-wide screening of broad-spectrum resistance to leaf rust (Puccinia triticina Eriks) in spring wheat (Triticum aestivum L.). Front. Plant Sci. 13:921230. https://doi.org/10.3389/fpls.2022.921230 Crossref, ISI, Google Scholar
- 2018. Genetic architecture of common bunt resistance in winter wheat using genome-wide association study. BMC Plant Biol. 18:280. https://doi.org/10.1186/s12870-018-1435-x Crossref, ISI, Google Scholar
- 2019b. Molecular marker dissection of stem rust resistance in Nebraska bread wheat germplasm. Sci. Rep. 9:11694. https://doi.org/10.1038/s41598-019-47986-9 Crossref, ISI, Google Scholar
- 2015. Small RNAs from the wheat stripe rust fungus (Puccinia striiformis f. sp. tritici). BMC Genomics 16:718. https://doi.org/10.1186/s12864-015-1895-4 Crossref, ISI, Google Scholar
- 2021. Uncovering genomic regions controlling plant architectural traits in hexaploid wheat using different GWAS models. Sci. Rep. 11:6767. https://doi.org/10.1038/s41598-021-86127-z Crossref, ISI, Google Scholar
- 2017. Moving nitrogen to the centre of plant defence against pathogens. Ann. Bot. 119:703‐709. https://doi.org/10.1093/aob/mcw179 ISI, Google Scholar
- 2019. Efficacy of certain bioagents on patho-physiological characters of wheat plants under wheat leaf rust stress. Physiol. Mol. Plant Pathol. 106:102‐108. https://doi.org/10.1016/j.pmpp.2018.12.010 Crossref, ISI, Google Scholar
- 1977. Partial resistance of barley to leaf rust, Puccinia hordei. IV. Effect of cultivar and development stage on infection frequency. Euphytica 26:249‐255. https://doi.org/10.1007/bf00026985 Crossref, ISI, Google Scholar
- 1975. Partial resistance of barley to leaf rust, Puccinia hordei. II. Relationship between field trials, micro plot tests and latent period. Euphytica 24:293‐303. https://doi.org/10.1007/bf00028194 Crossref, ISI, Google Scholar
- 2019. Accumulating evidences of callose priming by indole-3-carboxylic acid in response to Plectospharella cucumerina. Plant Signal. Behav. 14:1608107. https://doi.org/10.1080/15592324.2019.1608107 Crossref, ISI, Google Scholar
- 2015. WheatExp: An RNA-seq expression database for polyploid wheat. BMC Plant Biol. 15:299. https://doi.org/10.1186/s12870-015-0692-1 Crossref, ISI, Google Scholar
- 2020. Commercial formulates of Trichoderma induce systemic plant resistance to Meloidogyne incognita in tomato and the effect is additive to that of the mi-1.2 resistance gene. Front. Microbiol. 10:3042. https://doi.org/10.3389/fmicb.2019.03042 Crossref, ISI, Google Scholar
- 2019. Stripe rust effector PstGSRE1 disrupts nuclear localization of ROS-promoting transcription factor TaLOL2 to defeat ROS-induced defense in wheat. Mol. Plant 12:1624‐1638. https://doi.org/10.1016/j.molp.2019.09.010 Crossref, ISI, Google Scholar
- 2013. An extracellular subtilase switch for immune priming in Arabidopsis. PLoS Pathog. 9:e1003445. https://doi.org/10.1371/journal.ppat.1003445 Crossref, ISI, Google Scholar
- 2020. Ribosomal protein QM/RPL10 positively regulates defence and protein translation mechanisms during nonhost disease resistance. Mol. Plant Pathol. 21:1481‐1494. https://doi.org/10.1111/mpp.12991 Crossref, ISI, Google Scholar
- 2011. Colonization of Arabidopsis roots by Trichoderma atroviride promotes growth and enhances systemic disease resistance through jasmonic acid/ethylene and salicylic acid pathways. Eur. J. Plant Pathol. 131:15‐26. https://doi.org/10.1007/s10658-011-9782-6 Crossref, ISI, Google Scholar
- 2015. Association mapping for frost tolerance using multi-parent advanced generation inter-cross (MAGIC) population in faba bean (Vicia faba L.). Genetica 143:501-514. https://doi.org/10.1007/s10709-015-9848-z Crossref, ISI, Google Scholar
- 2018. Genetic variation in drought tolerance at seedling stage and grain yield in low rainfall environments in wheat (Triticum aestivum L.). Euphytica 214:169. https://doi.org/10.1007/s10681-018-2245-9 Crossref, ISI, Google Scholar
- 2017. Screening winter wheat lines in Nebraska for the Fhb1 gene using kompetitive allele specific PCR (KASP). J. Plant Genet. Breed. 1:1-4. Retrieved 14 March 2021 from https://www.omicsonline.org/open-access/screening-winter-wheat-lines-in-nebraska-for-the-fhb1-gene-usingkompetitive-allele-specific-pcr-kasp.pdf Google Scholar
- 2013. Effectiveness of biological control of Phytophthora capsici in pepper by Trichoderma asperellum strain T34. Phytopathol. Mediterr. 52:77‐83. https://doi.org/10.14601/Phytopathol_Mediterr-11242 ISI, Google Scholar
- 2010. Trichoderma asperellum strain T34 controls Fusarium wilt disease in tomato plants in soilless culture through competition for iron. Microb. Ecol. 59:141‐149. https://doi.org/10.1007/s00248-009-9545-5 Crossref, ISI, Google Scholar
- 2007. Proteome, salicylic acid, and jasmonic acid changes in cucumber plants inoculated with Trichoderma asperellum strain T34. Proteomics 7:3943‐3952. https://doi.org/10.1002/pmic.200700173 Crossref, ISI, Google Scholar
- 2009. MYB72, a node of convergence in induced systemic resistance triggered by a fungal and a bacterial beneficial microbe. Plant Biol. 11:90‐96. https://doi.org/10.1111/j.1438-8677.2008.00162.x Crossref, ISI, Google Scholar
- 2014. Negative control of BAK1 by protein phosphatase 2A during plant innate immunity. EMBO J. 33:2069‐2079. https://doi.org/10.15252/embj.201488698 Crossref, ISI, Google Scholar
- 2009. Subcellular localization and functional analysis of the Arabidopsis GTPase RabE. Plant Physiol. 149:1824‐1837. https://doi.org/10.1104/pp.108.132092 Crossref, ISI, Google Scholar
- 1962. Identification of Physiologic Races of Puccinia graminis var. tritici. United States Department of Agriculture–Agricultural Research Service, Washington, D.C. Google Scholar
- 2015. Native isolates of Trichoderma harzianum inducting resistance to Zymoseptoria tritici on wheat plants. Bol. Soc. Argent. Bot. 50:291‐301. https://doi.org/10.31055/1851.2372.v50.n3.12519 Crossref, ISI, Google Scholar
- 2019. Centromere satellite repeats have undergone rapid changes in polyploid wheat subgenomes. Plant Cell 31:2035‐2051. https://doi.org/10.1105/tpc.19.00133 Crossref, ISI, Google Scholar
- 2020. Unravelling the roles of nitrogen nutrition in plant disease defences. Int. J. Mol. Sci. 21:572. https://doi.org/10.3390/ijms21020572 Crossref, ISI, Google Scholar
- 2020. Fungi vs. fungi in biocontrol: An overview of fungal antagonists applied against fungal plant pathogens. Front. Cell Infect. Microbiol. 10:604923. https://doi.org/10.3389/fcimb.2020.604923 Crossref, ISI, Google Scholar
- 2016. Genome-wide association study on stem rust resistance in Kazakh spring barley lines. BMC Plant Biol. 16:6. https://doi.org/10.1186/s12870-015-0686-z Crossref, ISI, Google Scholar
- 1997. PLABSTAT: A computer program for statistical analysis of plant breeding experiments. https://docplayer.net/130759650-Plabstat-a-computer-program-for-statistical-analysis-of-plant-breeding-experiments-version-3a-pre-of-h-f-utz.html Google Scholar
- 2022. Seed coating with Trichoderma harzianum T-22 of Italian durum wheat increases protection against Fusarium culmorum induced crown rot. Agriculture 12:714. https://doi.org/10.3390/agriculture12050714 Crossref, Google Scholar
- 2009. Salicylic acid, a multifaceted hormone to combat disease. Annu. Rev. Phytopathol. 47:177‐206. https://doi.org/10.1146/annurev.phyto.050908.135202 Crossref, ISI, Google Scholar
- 2018. Pipecolic acid confers systemic immunity by regulating free radicals. Sci. Adv. 4:eaar4509. https://doi.org/10.1126/sciadv.aar4509 Crossref, ISI, Google Scholar
- 2022. Versatile physiological functions of the Nudix hydrolase family in berry development and stress response in grapevine. J. Integr. Agric. 21:91‐112. https://doi.org/10.1016/S2095-3119(20)63490-6 Crossref, ISI, Google Scholar
- 2012. Wheat BAX inhibitor-1 contributes to wheat resistance to Puccinia striiforms. J. Exp. Bot. 63:4571‐4584. https://doi.org/10.1093/jxb/ers140 Crossref, ISI, Google Scholar
- 2011. Global status of stripe rust: A review of historical and current threats. Euphytica 179:129‐141. https://doi.org/10.1007/s10681-011-0360-y Crossref, ISI, Google Scholar
- 2019. Defence priming in Arabidopsis—A meta-analysis. Sci. Rep. 9:13309. https://doi.org/10.1038/s41598-019-49811-9 Crossref, ISI, Google Scholar
- 2011. RNA-binding proteins in plant immunity. J. Pathog. 2011. https://doi.org/10.4061/2011/278697 Crossref, Google Scholar
- 2021. rMVP: A memory-efficient, visualization-enhanced, and parallel-accelerated tool for genome-wide association study. Genomics Proteomics Bioinf. 19:619-628. https://doi.org/10.1016/j.gpb.2020.10.007 Crossref, ISI, Google Scholar
- 2018. QTL mapping and validation of adult plant resistance to stripe rust in Chinese wheat landrace Humai 15. Front. Plant Sci. 9:968. https://doi.org/10.3389/fpls.2018.00968 Crossref, ISI, Google Scholar
- 2008. Isolasi dan Uji antagonis Jamur endofit akar Kelapa sawit (Elaeis guineensis Jacq.) terhadap Ganoderma boninense Pat. J. Biol. Sumatera 3:36‐41. Google Scholar
- 2020. Characterization of the heavy-metal-associated isoprenylated plant protein (Hipp) gene family from Triticeae species. Int. J. Mol. Sci. 21:6191. https://doi.org/10.3390/ijms21176191 Crossref, ISI, Google Scholar
- 2016. Application of plant-growth-promoting fungi Trichoderma longibrachiatum T6 enhances tolerance of wheat to salt stress through improvement of antioxidative defense system and gene expression. Front. Plant Sci. 7:1405. https://doi.org/10.3389/fpls.2016.01405 ISI, Google Scholar
- 2015. Isolation and characterisation of cDNA encoding a wheat heavy metal-associated isoprenylated protein involved in stress responses. Plant Biol. 17:1176‐1186. https://doi.org/10.1111/plb.12344 Crossref, ISI, Google Scholar
- 2020. Genetic network between leaf senescence and plant immunity: Crucial regulatory nodes and new insights. Plants 9:495. https://doi.org/10.3390/plants9040495 Google Scholar
- 1998. Elicitor-induced chloride efflux and anion channels in tobacco cell suspensions. Plant Physiol. Biochem. 36:665‐674. https://doi.org/10.1016/s0981-9428(98)80015-6 Crossref, ISI, Google Scholar