Divide and rule, or how plant diversity enhances the sustainability of their resistance

Yuanyang rice terraces in China. © INRA, JB Morel
Yuanyang rice terraces in China. © INRA, JB Morel

In the Yuanyang region of China where rice cultivation is a tradition, scientists from INRA and CIRAD, working in collaboration with a Chinese team, have focused on the defence mechanisms of rice against its pathogenic agents. They have shown how the very differing immune systems of two rice varieties that have been co-cultivated for centuries have united their forces to evade pathogenic agents in a sustainable manner. Published in eLIFE, these findings underline the importance of the functional diversity of plants to limiting epidemics at the scale of a landscape.

Plant pathogens constitute a threat to global food security. For example, the Magnaporthe oryzae fungus (which causes rice blast disease) devastates rice fields throughout the world, each year destroying crops that could feed more than 60 million people. Faced with this threat, the plants have developed several strategies. Their first line of defence is basal immunity through a certain number of antimicrobial responses. To evade this immunity, the pathogenic agents therefore deploy an arsenal of proteins (effectors). But the plants have also developed another defence strategy: resistance genes that are capable of detecting these effectors and then blocking microbial invasion more efficiently. Nevertheless, the pathogens are able to adapt their weapons and soon overcome these resistance genes, leading to an arms race.

The enigma of the Yuanyang rice fields

In south-western China, the Yuanyang rice fields extend over more than 10,000 hectares and have been recognised as a UNESCO World Heritage Site. In this region, where the farmers use no fungicides, the rice fields are astonishingly protected from epidemics. Why, and how? Scientists from the INRA-CIRAD-Montpellier SupAgro Joint Research Unit for the Biology and Genetics of Plant-Pathogen Interactions, and from the Yunnan Agricultural University in China, have tried to solve this mystery. Although the presence of Magnaporthe oryzae has been proved in these rice fields, they are very little affected by the fungus. Two rice varieties are cultivated there: ordinary rice (Indica) and sticky rice used for special occasions (Japonica). The scientists have been able to show that Japonica varieties display strong basal immunity and few resistance genes while conversely, Indica varieties possess weak basal immunity and numerous resistance genes.

Ultra-specialised pathogens

These two types of rice with such different immune systems have led to the existence of two specialised populations of fungi that can infect specific rice varieties. These two armies of ultra-specialised pathogens are therefore incapable of fighting on all fronts (even if on some plots a few battles have been lost by the plants), so that the fungus is prevented from spreading throughout the landscape.

Part of the "Eternal Rice" project team in the field (Yuanyang rice terraces, Yunnan, China). Development within this landscape of the disease caused by the pathogenic fungus Magnaporthe oryzae is prevented by the deployment of different immune systems. © Cirad, H. Adreit This study thus establishes a link between two of the articles in plant biology that have been the most frequently cited during the past fifteen years1. The first concerned a model for plant immunity (the zig-zag model) which predicts that an appropriate combination of basal immunity and resistance genes could increase the sustainability of resistance, while the second described an example in rice of the successful use of plant diversity as a driver of sustainable resistance against rice blast disease.

These initial findings of the Eternal Rice project have thus shown that the deployment of diversified immune systems can enable the development of agroecosystems characterised by sustainable plant protection. The scientists will now be carrying out similar experiments on wheat crops.

The Eternal Rice project

This work was carried out in the context of the Eternal Rice project, which forms part of the SMaCH metaprogramme (Sustainable Management of Crop Health) set up by INRA. The Eternal Rice project involves the INRA-CIRAD-Montpellier SupAgro Joint Research Unit for the Biology and Genetics of Plant-Pathogen Interactions and the Yunnan Agricultural University in China. Other groups are also participating in the project: from the INRA-AgroParisTech Joint Research Unit: Science for Action and Sustainable Development: Activities, Products, Territories; INRA’s Biostatistics and Spatial Processes Research Unit and the INRA-Bordeaux Sciences Agro Joint Research Unit for Vine Health and Agroecology. Launched in 2014, this project aims to study the sustainable management of varietal resistance in rice in the Yuanyang rice fields of southern Yunnan, which are a UNESCO World Heritage Site. This project combines the use of methods in genetics, genomics, the analysis of social networks and modelling.

1. Jones JD, Dangl JL. The plant immune system. Nature (2006) 444(7117):323-9 and Zhu Y, Chen H, Fan J, Wang Y, Li Y, Chen J, Fan J, Yang S, Hu L, Leung H, Mew TW, Teng PS, Wang Z, Mundt CC. Genetic diversity and disease control in rice. Nature (2000) 406(6797):718-22

Pathogen effectors and plant immunity determine specialization of the blast fungus to rice subspecies. LIAO Jingjing, HUANG Huichuan, MEUSNIER Isabelle, ADREIT Henri, DUCASSE Aurélie, BONNOT François, PAN Lei, HE Xiahong, KROJ Thomas, FOURNIER Elisabeth, THARREAU Didier, GLADIEUX Pierre, Jean-Benoit MOREL. eLIFE. 23 December 2016. DOI : http://dx.doi.org/10.7554/e­Life.19377