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1. Extensive immune receptor repertoire diversity in disease-resistant rice landraces.

Author

Gladieux P, van Oosterhout C, Fairhead S, Jouet A, Ortiz D, Ravel S, Shrestha RK, Frouin J, He X, Zhu Y, Morel JB, Huang H, Kroj T, and Jones JDG

Subjects
NLR Proteins genetics, NLR Proteins metabolism, Plant Proteins genetics, Plant Proteins metabolism, Receptors, Immunologic genetics, Receptors, Immunologic metabolism, China, Haplotypes, Ascomycota, Oryza genetics, Oryza immunology, Oryza microbiology, Plant Diseases microbiology, Plant Diseases genetics, Plant Diseases immunology, Disease Resistance genetics, Genetic Variation
Abstract

Plants have powerful defense mechanisms and extensive immune receptor repertoires, yet crop monocultures are prone to epidemic diseases. Rice (Oryza sativa) is susceptible to many diseases, such as rice blast caused by Magnaporthe oryzae. Varietal resistance of rice to blast relies on intracellular nucleotide binding, leucine-rich repeat (NLR) receptors that recognize specific pathogen molecules and trigger immune responses. In the Yuanyang terraces in southwest China, rice landraces rarely show severe losses to disease whereas commercial inbred lines show pronounced field susceptibility. Here, we investigate within-landrace NLR sequence diversity of nine rice landraces and eleven modern varieties using complexity reduction techniques. We find that NLRs display high sequence diversity in landraces, consistent with balancing selection, and that balancing selection at NLRs is more pervasive in landraces than modern varieties. Notably, modern varieties lack many ancient NLR haplotypes that are retained in some landraces. Our study emphasizes the value of standing genetic variation that is maintained in farmer landraces as a resource to make modern crops and agroecosystems less prone to disease. The conservation of landraces is, therefore, crucial for ensuring food security in the face of dynamic biotic and abiotic threats., Competing Interests: Declaration of interests The authors declare no competing interests, (Copyright © 2024 The Authors. Published by Elsevier Inc. All rights reserved.)

Published
2024
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2. Phytoalexin sakuranetin attenuates endocytosis and enhances resistance to rice blast.

Author

Jiang L, Zhang X, Zhao Y, Zhu H, Fu Q, Lu X, Huang W, Yang X, Zhou X, Wu L, Yang A, He X, Dong M, Peng Z, Yang J, Guo L, Wen J, Huang H, Xie Y, Zhu S, Li C, He X, Zhu Y, Friml J, and Du Y

Subjects
Sesquiterpenes pharmacology, Sesquiterpenes metabolism, Gene Expression Regulation, Plant drug effects, Cell Membrane metabolism, Cell Membrane drug effects, Plants, Genetically Modified, Fungal Proteins metabolism, Fungal Proteins genetics, Oryza microbiology, Oryza metabolism, Oryza drug effects, Oryza genetics, Plant Diseases microbiology, Endocytosis drug effects, Phytoalexins, Disease Resistance genetics, Disease Resistance drug effects, Plant Proteins metabolism, Plant Proteins genetics, Ascomycota, Flavonoids
Abstract

Phytoalexin sakuranetin functions in resistance against rice blast. However, the mechanisms underlying the effects of sakuranetin remains elusive. Here, we report that rice lines expressing resistance (R) genes were found to contain high levels of sakuranetin, which correlates with attenuated endocytic trafficking of plasma membrane (PM) proteins. Exogenous and endogenous sakuranetin attenuates the endocytosis of various PM proteins and the fungal effector PWL2. Moreover, accumulation of the avirulence protein AvrCO39, resulting from uptake into rice cells by Magnaporthe oryzae, was reduced following treatment with sakuranetin. Pharmacological manipulation of clathrin-mediated endocytic (CME) suggests that this pathway is targeted by sakuranetin. Indeed, attenuation of CME by sakuranetin is sufficient to convey resistance against rice blast. Our data reveals a mechanism of rice against M. oryzae by increasing sakuranetin levels and repressing the CME of pathogen effectors, which is distinct from the action of many R genes that mainly function by modulating transcription., (© 2024. The Author(s).)

Published
2024
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3. Emergence of Southern Rice Black-Streaked Dwarf Virus in the Centuries-Old Chinese Yuanyang Agrosystem of Rice Landraces.

Author

Alonso P, Gladieux P, Moubset O, Shih PJ, Mournet P, Frouin J, Blondin L, Ferdinand R, Fernandez E, Julian C, Filloux D, Adreit H, Fournier E, Ducasse A, Grosbois V, Morel JB, Huang H, Jin B, He X, Martin DP, Vernière C, and Roumagnac P

Subjects
China, Communicable Diseases, Emerging virology, Japan, Phylogeny, Reoviridae classification, Reoviridae genetics, Vietnam, Oryza virology, Plant Diseases virology, Reoviridae isolation & purification
Abstract

Southern rice black-streaked dwarf virus (SRBSDV), which causes severe disease symptoms in rice ( Oriza sativa L.) has been emerging in the last decade throughout northern Vietnam, southern Japan and southern, central and eastern China. Here we attempt to quantify the prevalence of SRBSDV in the Honghe Hani rice terraces system (HHRTS)-a Chinese 1300-year-old traditional rice production system. We first confirm that genetically diverse rice varieties are still being cultivated in the HHRTS and categorize these varieties into three main genetic clusters, including the modern hybrid varieties group (MH), the Hongyang improved modern variety group (HY) and the traditional indica landraces group (TIL). We also show over a 2-year period that SRBSDV remains prevalent in the HHRTS (20.1% prevalence) and that both the TIL (17.9% prevalence) and the MH varieties (5.1% prevalence) were less affected by SRBSDV than were the HY varieties (30.2% prevalence). Collectively we suggest that SRBSDV isolates are freely moving within the HHRTS and that TIL, HY and MH rice genetic clusters are not being preferentially infected by particular SRBSDV lineages. Given that SRBSDV can cause 30-50% rice yield losses, our study emphasizes both the need to better monitor the disease in the HHRTS, and the need to start considering ways to reduce its burden on rice production.

Published
2019
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4. Pathogen effectors and plant immunity determine specialization of the blast fungus to rice subspecies.

Author

Liao J, Huang H, Meusnier I, Adreit H, Ducasse A, Bonnot F, Pan L, He X, Kroj T, Fournier E, Tharreau D, Gladieux P, and Morel JB

Subjects
Host-Pathogen Interactions, Magnaporthe physiology, Host Specificity, Magnaporthe pathogenicity, Oryza immunology, Oryza microbiology, Plant Diseases microbiology, Plant Immunity, Virulence Factors metabolism
Abstract

Understanding how fungi specialize on their plant host is crucial for developing sustainable disease control. A traditional, centuries-old rice agro-system of the Yuanyang terraces was used as a model to show that virulence effectors of the rice blast fungus Magnaporthe oryzaeh play a key role in its specialization on locally grown indica or japonica local rice subspecies. Our results have indicated that major differences in several components of basal immunity and effector-triggered immunity of the japonica and indica rice varieties are associated with specialization of M. oryzae . These differences thus play a key role in determining M. oryzae host specificity and may limit the spread of the pathogen within the Yuanyang agro-system. Specifically, the AVR-Pia effector has been identified as a possible determinant of the specialization of M. oryzae to local japonica rice., Competing Interests: The authors declare that no competing interests exist.

Published
2016
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5. Heterogeneity of the rice microbial community of the Chinese centuries-old Honghe Hani rice terraces system

Author

Alonso, Pascal, Blondin, Laurence, Gladieux, Pierre, Mahé, Frédéric, Sanguin, Hervé, Ferdinand, Romain, Filloux, Denis, Desmarais, Eric, Cerqueira, Frédérique, Jin, Baihui, Huang, Huichuan, He, Xiahong, Morel, Jean-Benoit, Martin, Darren Patrick, Roumagnac, Philippe, Vernière, Christian, Biologie et Génétique des Interactions Plante-Parasite (UMR BGPI), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut Agro - Montpellier SupAgro, Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro), Département Systèmes Biologiques (Cirad-BIOS), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad), Institut des Sciences de l'Evolution de Montpellier (UMR ISEM), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-École Pratique des Hautes Études (EPHE), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Université de Montpellier (UM)-Institut de recherche pour le développement [IRD] : UR226-Centre National de la Recherche Scientifique (CNRS), Yunnan Agricultural University, Southwest Forestry University (SWFU), University of Cape Town, French International and Agricultural Research Agency (CIRAD), Agropolis Fondation (E-Space Flagship Program) : 1504-004, CGIAR Research Program (CRP) on rice agri-food systems (RICE)Yunnan Agricultural University, International Associated Laboratory Plantomix (INRAE/Yunnan Agricultural University), National Research Foundation - South Africa, ANR-17-CE32-0011,NGB,Biosurveillance Next-Gen des changements dans la structure et le fonctionnement des écosystèmes(2017), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), École pratique des hautes études (EPHE), and Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Université de Montpellier (UM)-Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Centre National de la Recherche Scientifique (CNRS)-Institut de recherche pour le développement [IRD] : UR226

Subjects
China, F40 - Écologie végétale, Flore microbienne, Rizière, F08 - Systèmes et modes de culture, Microbiota, [SDV]Life Sciences [q-bio], food and beverages, Oryza sativa, Agriculture, Oryza, Biodiversity, Culture en terrasse, Humans, Écologie microbienne, Research Articles, Plant Diseases, Research Article
Abstract

BGPI : équipe 4, 5, 7; The Honghe Hani rice terraces system (HHRTS) is a traditional rice cultivation system where Hani people cultivate remarkably diverse rice varieties. Recent introductions of modern rice varieties to the HHRTS have significantly increased the severity of rice diseases within the terraces. Here, we determine the impacts of these recent introductions on the composition of the rice-associated microbial communities. We confirm that the HHRTS contains a range of both traditional HHRTS landraces and introduced modern rice varieties and find differences between the microbial communities of these two groups. However, this introduction of modern rice varieties has not strongly impacted the overall diversity of the HHRTS rice microbial community. Furthermore, we find that the rice varieties (i.e. groups of closely related genotypes) have significantly structured the rice microbial community composition (accounting for 15%-22% of the variance) and that the core microbial community of HHRTS rice plants represents less than 3.3% of all the microbial taxa identified. Collectively, our study suggests a highly diverse HHRTS rice holobiont (host with its associated microbes) where the diversity of rice hosts mirrors the diversity of their microbial communities. Further studies will be needed to better determine how such changes might impact the sustainability of the HHRTS.

Published
2020

6. Emergence of southern rice black-streaked dwarf virus in the centuries-old Chinese Yuanyang agrosystem of rice landraces

Author

Alonso, Pascal, Gladieux, Pierre, Moubset, Oumaima, Shih, Pei-Jung, MOURNET, Pierre, Frouin, Julien, Blondin, Laurence, Ferdinand, Romain, Fernandez, Emmanuel, Julian, Charlotte, Filloux, Denis, Adreit, Henri, Fournier, Elisabeth, Ducasse, Aurélie, Grosbois, Vladimir, Morel, Jean-Benoit, Huang, Huichuan, Jin, Baihui, He, Xiahong, Martin, Darren P., Vernière, Christian, Roumagnac, Philippe, Biologie et Génétique des Interactions Plante-Parasite (UMR BGPI), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Institut National de la Recherche Agronomique (INRA)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro), National Chung Hsing University, Amélioration génétique et adaptation des plantes méditerranéennes et tropicales (UMR AGAP), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Institut National de la Recherche Agronomique (INRA)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro), Animal, Santé, Territoires, Risques et Ecosystèmes (UMR ASTRE), Institut National de la Recherche Agronomique (INRA)-Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad), State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural University, Southwest Forestry University (SWFU), Computational Biology Group, Institute of Infectious Diseases and Molecular Medicine, University of Cape Town, Agropolis Fondation (E-Space flagship program) : 1504-004, and National Research Foundation - South Africa

Subjects
[SDV.SA]Life Sciences [q-bio]/Agricultural sciences, China, host genotyping, lcsh:QR1-502, Honghe Hani rice terraces system, Oryza sativa, Reoviridae, Communicable Diseases, Emerging, lcsh:Microbiology, Article, Japan, Variété indigène, Culture en terrasse, Phylogeny, Plant Diseases, H20 - Maladies des plantes, Southern rice black-streaked dwarf virus, rice, virus emergence, virus prevalence, food and beverages, Oryza, Virus des végétaux, Rice black streaked dwarf virus [EN], Agricultural sciences, Vietnam, maladie virale, Sciences agricoles
Abstract

Southern rice black-streaked dwarf virus (SRBSDV), which causes severe disease symptoms in rice (Oriza sativa L.) has been emerging in the last decade throughout northern Vietnam, southern Japan and southern, central and eastern China. Here we attempt to quantify the prevalence of SRBSDV in the Honghe Hani rice terraces system (HHRTS)&mdash, a Chinese 1300-year-old traditional rice production system. We first confirm that genetically diverse rice varieties are still being cultivated in the HHRTS and categorize these varieties into three main genetic clusters, including the modern hybrid varieties group (MH), the Hongyang improved modern variety group (HY) and the traditional indica landraces group (TIL). We also show over a 2-year period that SRBSDV remains prevalent in the HHRTS (20.1% prevalence) and that both the TIL (17.9% prevalence) and the MH varieties (5.1% prevalence) were less affected by SRBSDV than were the HY varieties (30.2% prevalence). Collectively we suggest that SRBSDV isolates are freely moving within the HHRTS and that TIL, HY and MH rice genetic clusters are not being preferentially infected by particular SRBSDV lineages. Given that SRBSDV can cause 30&ndash, 50% rice yield losses, our study emphasizes both the need to better monitor the disease in the HHRTS, and the need to start considering ways to reduce its burden on rice production.

Published
2019

7. The Phytophthora cactorum genome provides insights into the adaptation to host defense compounds and fungicides

Author

Huang Huichuan, Wei Wei, Xili Liu, Yang Dong, Ting Yang, Mei Xinyue, Shengchang Duan, Xiahong He, Liu Yixiang, Min Yang, Shusheng Zhu, Cunwu Guo, and Wei Chen

Subjects
Phytophthora, 0106 biological sciences, 0301 basic medicine, Phytophthora cactorum, Secondary Metabolism, lcsh:Medicine, 01 natural sciences, Genome, Article, Host-Parasite Interactions, 03 medical and health sciences, Author Correction, lcsh:Science, Gene, Plant Diseases, Oomycete, Genetics, Multidisciplinary, biology, Host (biology), Effector, lcsh:R, Proteins, Plants, biology.organism_classification, Adaptation, Physiological, Fungicides, Industrial, Fungicide, 030104 developmental biology, lcsh:Q, 010606 plant biology & botany
Abstract

Phytophthora cactorum is a homothallic oomycete pathogen, which has a wide host range and high capability to adapt to host defense compounds and fungicides. Here we report the 121.5 Mb genome assembly of the P. cactorum using the third-generation single-molecule real-time (SMRT) sequencing technology. It is the second largest genome sequenced so far in the Phytophthora genera, which contains 27,981 protein-coding genes. Comparison with other Phytophthora genomes showed that P. cactorum had a closer relationship with P. parasitica, P. infestans and P. capsici. P. cactorum has similar gene families in the secondary metabolism and pathogenicity-related effector proteins compared with other oomycete species, but specific gene families associated with detoxification enzymes and carbohydrate-active enzymes (CAZymes) underwent expansion in P. cactorum. P. cactorum had a higher utilization and detoxification ability against ginsenosides–a group of defense compounds from Panax notoginseng–compared with the narrow host pathogen P. sojae. The elevated expression levels of detoxification enzymes and hydrolase activity-associated genes after exposure to ginsenosides further supported that the high detoxification and utilization ability of P. cactorum play a crucial role in the rapid adaptability of the pathogen to host plant defense compounds and fungicides.

Published
2018

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