Phosphate excess increases susceptibility to pathogen infection in rice

Abstract

Phosphorus (P) is an essential nutrient for plant growth and productivity. Due to soil fixation, however, phosphorus availability in soil is rarely sufficient to sustain high crop yields. The overuse of fertilizers to circumvent the limited bioavailability of phosphate (Pi) has led to a scenario of excessive soil P in agricultural soils. Whereas adaptive responses to Pi deficiency have been deeply studied, less is known about how plants adapt to Pi excess and how Pi excess might affect disease resistance. We show that high Pi fertilization, and subsequent Pi accumulation, enhances susceptibility to infection by the fungal pathogen Magnaporthe oryzae in rice. This fungus is the causal agent of the blast disease, one of the most damaging diseases of cultivated rice worldwide. Equally, MIR399f overexpression causes an increase in Pi content in rice leaves, which results in enhanced susceptibility to M. oryzae. During pathogen infection, a weaker activation of defence‐related genes occurs in rice plants over‐accumulating Pi in leaves, which is in agreement with the phenotype of blast susceptibility observed in these plants. These data support that Pi, when in excess, compromises defence mechanisms in rice while demonstrating that miR399 functions as a negative regulator of rice immunity. The two signalling pathways, Pi signalling and defence signalling, must operate in a coordinated manner in controlling disease resistance. This information provides a basis to understand the molecular mechanisms involved in immunity in rice plants under high Pi fertilization, an aspect that should be considered in management of the rice blast disease.

Crosstalk between Nutrient Signalling Pathways and Immune Responses in Rice

“…Recent studies have demonstrated that the miR399 might function as a potential integrator of Pi starvation responses and immune-defence responses in rice plants. Thus, transgenic rice plants overexpressing miR399 showed increased phosphate content, weaker induction of defence-related genes, and enhanced susceptibility to M. oryzae, which also correlates with the susceptibility phenotype observed in rice plants grown in Pi excess conditions [98]. Other components of the Pi starvation signalling also regulate the expression of genes involved in immune responses [121,122].…”

“…oryzae interaction (Figure 2). Some of these miRNAs function as positive regulators of immune responses (miR7695, miR160a, miR162a, miR398b, miR166k-166h and miR812w), whereas other miRNAs function as negative regulators of rice immune responses (miR156fhl, miR164a, miR167d, miR169a, miR319b, miR396, miR399, miR444b.2, miR439, and miR1873) [77,[98][99][100][101][102][103][104][105][106][107][108][109]. To note, miR398 has been reported to function as a positive regulator of immune responses in rice against M. oryzae while negatively regulating immune responses against P. syringae in Arabidopsis [110].…”

“…In rice, high nitrogen (N) supply not only promotes M. oryzae growth but also induces the expression of fungal effector genes, thus making the plant more susceptible to infection [117]. Growing rice plants under high phosphate (Pi) conditions leads to an increase in leaf Pi content, which is associated with a weaker activation of defence responses and susceptibility against the rice blast fungus [98]. Ferroptosis, an iron (Fe)-and ROS-dependent cell death process, contributes to arrest M. oryzae infection in incompatible rice/M.…”

“…However, our knowledge of interactions between plant adaptive mechanisms to Pi excess and immunity is still limited. Only recently, it was described that high Pi fertilisation compromises the expression of immune responses and enhances susceptibility to infection by M. oryzae in rice plants [98] (Figure 3). In other studies, overexpression of the OsPT8 phosphate transporter, and subsequent increase in Pi content, was reported to enhance susceptibility to M. oryzae infection [123].…”

Role of transporters in plant disease resistance

“…Oryzae , indicating the possible cross‐talk between OsPT8 , Pi signaling, and plant immunity (Dong et al, 2019). The excess of Pi enhances disease susceptibility to M. oryzae in rice, indicating the importance of coordination between Pi and defense signaling (Campos‐Soriano et al, 2020).…”