Rice (Oryza sativa L) is the most important cereal crop cultivated in the world and, to maintain the required levels of productivity, high amounts of phosphate fertilizers are routinely used, leading to a scenario of phosphate excess in agricultural soils. A recently published work led by CRAG researchers has revealed that rice plants, when grown in soil with an excess of phosphate, are more susceptible to infection by the fungal pathogen Magnaporthe oryzae, which causes the very damaging blast disease. The study, led by the CSIC Research Professor at CRAG Blanca San Segundo, has been published in the journal Molecular Plant Pathology.

“The negative impact for the environment of phosphate excess in soils was already known, but now we have discovered that it can also have a negative impact on crops grown in high phosphate soil”, explains San Segundo.

High phosphate content in soil increases disease susceptibility

During decades, agriculture practices have been compensating the low bioavailability of phosphate, an essential nutrient for plant growth, by the massive application of fertilizers. This led to the actual situation where most of the cultivated lands present phosphate excess, which causes environmental problems due to soil pollution and water eutrophication, and raises serious concerns about food safety and animal health.

Rice is the staple food for more than half of the world's population. However, rice production is severely threatened by the blast disease caused by the fungal pathogen Magnaporthe oryzae. This disease has been reported in more than 80 countries on all continents where rice is grown, and the fungus is estimated to destroy enough rice to feed more than 60 million people each year.

To evaluate how phosphate supply influences blast disease resistance in rice, Blanca San Segundo’s team and collaborators from the Agricultural Biotechnology Research Center-Academia Sinica (Taiwan) grew different rice cultivars under different inorganic phosphate –the form of phosphate found in fertilizers– regimes (low, sufficient and high

 

 

“We found that high phosphate fertilization, and subsequent phosphate accumulation in rice leaves, increased susceptibility to infection by the fungus Magnaporthe oryzae” explains Lidia Campos-Soriano, co-first author of the research article.

The researchers analysed gene expression under the different phosphate conditions and observed that phosphate accumulation negatively affects defence gene expression during pathogen infection, which could explain the susceptibility observed. 

“The take home message of the study is that the indiscriminate use of fertilizers, in addition to cause environmental problems, might cause unintended effects in rice farming by facilitating pathogen infection. Phosphate fertilization should then be considered on a cost–benefit basis in rice farming. The results presented here might lay a foundation for a more rational and efficient use of fertilizers and pesticides in rice cultivation” explains the lead researcher Blanca San Segundo.

A 2008 report from the FAO recommended the efficient use of fertilizer phosphorus for three main reasons: 1) because phosphate rock, from which phosphorus fertilizers are manufactured, is a finite, non-renewable resource; 2) for the need to increase food production and improve rural livelihoods; and 3) to avoid undesirable changes in the aquatic ecosystems produced by the transfer of soil phosphate to surface waters. The findings recently reported by CRAG and Academia Sinica researchers add a fourth reason for the efficient use of inorganic phosphorous.

A microRNA involved in phosphate responses regulates defence gene expression

To investigate the mechanisms by which phosphate accumulation enhances rice susceptibility to blast disease, researchers generated rice plants overexpressing miR399, a microRNA known to be involved in plant responses to phosphate starvation.

“We discovered that this genetically-modified plants were more susceptible to Magnaporthe oryzae infection than their wild-type counterparts”, explains Mireia Bundó, who is also co-first author of the work.

Further experiments revealed that miR399 overexpression affected the expression of genes involved in protein phosphorylation as well as in the plant defence responses. Under pathogen challenge, a weaker induction of defence gene expression was observed in miR399 overexpressing rice plants, which correlated well with their enhanced disease susceptibility phenotype.

The results clearly support a link between phosphate signalling and the immune signalling response in rice plants.

Further steps to deal with the problem

Nutrient and pathogen stresses induce signalling pathways that might interact, in a synergistic or antagonistic way, determining resistance or susceptibility to pathogen infection. While numerous studies focus on the molecular mechanisms involved in the plant response to phosphate limiting conditions, mostly in the model plant Arabidopsis thaliana, less attention has been paid to understand how crop species cope with phosphate excess, which highlights the importance of the study led by San Segundo.

“Further investigation is needed to understand how signals coming from the two types of stresses, phosphate excess and pathogen infection, are integrated during pathogen infection” concludes Blanca San Segundo.

 

Reference article: Campos-Soriano, L., Bundó, M., Bach-Pages, M., Chiang, S.-F., Chiou, T.-J., San Segundo, B. Phosphate excess increases susceptibility to pathogen infection in rice. Molecular Plant Pathology. (2020) , vol. 21 (4), pp. 555 -570 (DOI:10.1111/mpp.12916)

About the the funding: This research was supported by the Spanish Ministerio de Ciencia, Innovación y Universidades (MCIU)‐Agencia Estatal de Investigación (AEI) & Fondo Europeo de Desarrollo Regional (FEDER), by the Generalitat de Catalunya and the Academia Sinica (Taiwan). M.B.P. was funded by a “la Caixa” scholarship for PhD studies in Spanish universities.