OsPGIP1-Mediated Resistance to Bacterial Leaf Streak in Rice is Beyond Responsive to the Polygalacturonase of Xanthomonas oryzae pv. oryzicola

Tao Wu,Xinhua Ding,Fuchuan Li,Fang Liu,Zhaohui Chu,Lingguang Kong,Beibei Li,Chune Peng,Wei Wu

doi:10.1186/s12284-019-0352-4

Abstract

Polygalacturonase-inhibiting proteins (PGIPs) have been shown to recognize fungal polygalacturonases (PGs), which initiate innate immunity in various plant species. Notably, the connection between rice OsPGIPs and PGs in Xanthomonas oryzae pv. oryzicola (Xoc), which causes bacterial leaf streak (BLS), remains unclear. Here, we show that OsPGIP1 was strongly induced after inoculating rice with the Xoc strain RS105. Furthermore, OsPGIP1-overexpressing (OV) and RNA interference (RNAi) rice lines increased and decreased, respectively, the resistance of rice to RS105, indicating that OsPGIP1 contributes to BLS resistance. Subsequently, we generated the unique PG mutant RS105Δpg, the virulence of which is attenuated compared to that of RS105. Surprisingly, the lesion lengths caused by RS105Δpg were similar to those caused by RS105 in the OV lines compared with wild-type ZH11 with reduced Xoc susceptibility. However, the lesion lengths caused by RS105Δpg were still significantly shorter in the OV lines than in ZH11, implying that OsPGIP1-mediated BLS resistance could respond to other virulence factors in addition to PGs. To explore the OsPGIP1-mediated resistance, RNA-seq analysis were performed and showed that many plant cell wall-associated genes and several MYB transcription factor genes were specifically expressed or more highly induced in the OV lines compared to ZH11 postinoculation with RS105. Consistent with the expression of the differentially expressed genes, the OV plants accumulated a higher content of jasmonic acid (JA) than ZH11 postinoculation with RS105, suggesting that the OsPGIP1-mediated resistance to BLS is mainly dependent on the plant cell wall-associated immunity and the JA signaling pathway.

Highlights

The battle between pathogens and plants, known as the “arms race”, is the result of millions of years of coevolution (Boller and He 2009)
We further investigated the difference in the expression of OsPGIP1 to OsPGIP7 between the susceptible variety ZH11 and the moderately resistant variety Acc8558
The expression patterns of OsPGIP2 and OsPGIP4 after inoculation with RS105 in Acc8558 were similar to those in ZH11, but the expression levels were even higher in Acc8558 (Additional file 7: Figure S1)

Summary

Introduction

The battle between pathogens and plants, known as the “arms race”, is the result of millions of years of coevolution (Boller and He 2009). Similar to the skin of animals, the plant cell surface is the first layer of physical and chemical protection against invading pathogens. This first protective layer includes the plant waxy cuticles and the release of plant metabolites that act as anti-microbial compounds (Jones and Dangl 2006; Malinovsky et al 2014). PGs are secreted by fungi, bacteria and insects at the early stage of infection and serve as a pathogenicity factor. This hydrolytic enzyme cleaves the α-(1–4) linkages between the D-galacturonic acid residues of homogalacturonan to degrade cell wall polysaccharides and facilitate the availability of host nutrients (Kalunke et al 2015; Bacete et al 2018)

Methods

Results

Conclusion