Rice blast, caused by the fungus Maganaporthe oryzae, is the most devastating rice disease resulting in the worldwide annual loss of 10–30% of the rice harvest, amount enough to feed approximately 60 million people. Deployment of resistance (R) genes in rice is considered as the best practice to manage diseases and curtail the environmental damage by reducing the use of agro-chemicals[1]. To date, more than 100 R genes have been identified in rice, and 25 of them have been cloned and characterized[2]. Although some R genes conferring strain-specific resistance have been applied in plant breeding, their effect can be rapidly overcome by the emergence of compatible blast isolates[1]. In addition, because pyramiding R genes to develop resistant cultivars is an extremely time-consuming process, rice production is still facing a huge threat caused by the fast evolution of pathogenic blast fungi[3]. Therefore, characterizing the molecular mechanism of durable and broad-spectrum resistance is important for guiding rice resistance breeding. Gumei 4 (GM4) and Digu, two Chinese Indica rice varieties, display high and durable blast resistance[4, 5]. Recent studies have shown that PigmR gene encoding nucleotide-binding leucine-rich repeat (NLR) receptor confers broad-spectrum resistance in GM4[4], and a single base change (SNP33-G) in the bsr-d1 (a natural allele of a C2H2-domain transcription factor gene) promoter enhances binding to MYBS1 and confers broad-spectrum resistance to rice blast in Digu[5].
The cultivated rice (Oryza sativa L.) is divided into two main subspecies: Japonica and indica. Because japonica rice has better taste quality than indica rice, the planting area in China is expanding year by year. However, compared with indica rice, the blast resistance of japonica rice is generally very poor[6]. In fact, most of the identified broad-spectrum blast resistance resources are indica rice, like Digu and Gumei, and the molecular mechanisms on broad-spectrum blast resistance characterized so far are limited to indica rice and these genes cloned from ndica rice materials. However, the resistance resources of japonica rice, especially those with broad-spectrum blast resistance, are relatively scarce, and the broad-spectrum resistance mechanism of japonica rice is still very little known, which is very unfavorable to the overall understanding of the molecular mechanism of broad-spectrum resistance to rice blast.
Plants employ a two-tier innate immunity system to protect them from a wide range of pathogens: pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI), and effector-triggered immunity (ETI)[7, 8]. PTI contributes to host defense against infections by a broad range of pathogens, activation of PTI leads to various immune responses, including calcium influx, the deposition of callose, a rapid burst of reactive oxygen species (ROS), and expression of defense genes[9]. These responses confer effective and broad-spectrum defense against the majority of potential pathogens. Downstream of PTI activation, the activation of complex phytohormones signaling networks is critical for stimulating plant innate immunity[10]. Salicylic acid (SA) and jasmonate (JA) are recognized as the most important hormones in plant immune responses and are believed to represent the hormonal backbone of defense against pathogens[11]. In general, the SA pathway is crucial for immune responses against biotrophic and hemibiotrophic pathogens, whereas the JA pathway is involved in defense against necrotrophic pathogens acquiring nutrients from the decaying host tissue[12, 13]. Moreover, interaction between these two types of defense is mostly antagonistic[12, 14, 15]. This reciprocal antagonistic crosstalk between the SA and JA pathways, initially demonstrated in Arabidopsis[16, 17], is present also in other plant species[18]. Nonetheless, evidence deviating of the antagonism between SA and JA also exists, particularly in monocotyledonous plants[19–22].
Ziyu44, a japonica rice variety of Yunnan Province, has broad-spectrum resistance to 16 physiological races (ZA1, ZA49, ZA57, ZA61, ZB1, ZB13, ZB17, ZB25, ZC1,ZC3, ZC13, ZC15, ZE1, ZE3, ZF1 and ZG1) from Yunnan province[23]. Over the past 30 years, field-cultivated Ziyu44 has displayed high and durable resistance to rice blast[24]. Our previous studies have identified a number of major and minor resistance genes in Ziyu44[24–26] and suggested that durable broad-spectrum resistance to rice blast in this cultivar may reflect a combined effect of multiple loci. However, the functions of SA and JA in regulating immunity in Ziyu44 are unclear. Specifically, the spatiotemporal dynamics of SA and JA during the interaction between Ziyu44 and M. oryzae, and the relative contribution of each hormone to the defense response of Ziyu44 remain unknown. Therefore, the objective of the present study was to compare appressorium formation, hypha growth, endogenous SA and JA content, and expression of SA- and JA-associated genes in Ziyu44 and JNXN rice varieties in response to M. oryzae infection. The obtained results revealed that the accumulation of JA and activation of the SA-JA defense signaling at the early stages of M. oryzae infection in the durably resistant rice Ziyu44 is essential for the resistance to rice blast.