Elsevier

Plant Physiology and Biochemistry

Volume 142, September 2019, Pages 106-116
Plant Physiology and Biochemistry

Research article
Strigolactones positively regulate defense against Magnaporthe oryzae in rice (Oryza sativa)

https://doi.org/10.1016/j.plaphy.2019.06.028Get rights and content

Highlights

  • Strigolactone (SL) synthesis and signaling enhance resistance against rice blast infection.

  • RNA-sequencing revealed SL-mediated defense-related genes/pathways against blast infection.

  • SLs may serve as a novel target to improve rice defense against blast infection.

Abstract

This study presents evidence that strigolactones (SLs) promote defense against devastating rice blast fungal pathogen Magnaporthe oryzae. Impairment in either SL-biosynthetic dwarf17 (d17) or –signaling (d14) led to increased susceptibility towards M. oryzae. Comparative transcriptome profiling of the SL-signaling d14 mutant and WT plants revealed that a large number of defense-associated genes including hydrogen peroxide (H2O2)-, ethylene- and cell wall-synthesis-related genes were remarkably suppressed in d14 with respect to that of WT plants, during M. oryzae infection. In addition, various KEGG metabolic pathways related to sugar metabolism were significantly suppressed in the d14 plants compared to WT, during M. oryzae infection. Accordingly, WT plants accumulated increased levels of H2O2 and soluble sugar content compared to that of d17 and d14 in response to M. oryzae infection. Altogether, these results propose that SLs positively regulated rice defense against M. oryzae through involvement in the induction of various defense associated genes/pathways.

Introduction

Rice (Oryza sativa L.) is among the important staple food crops, fulfilling food requirements of about half of the world human population (Dean et al., 2012; Nasir et al., 2018). The global human population is expected to increase to around 9.2 billion at 2050; and, thus to feed this increased population, enhancement in the yield of rice is extremely essential. Unfortunately, rice blast disease caused by the hemibiotrophic fungal pathogen, Magnaporthe oryzae, results in approximately 10–30% damage to the rice harvest world-wide per annum, which therefore remains a major threat to food security globally (Dean et al., 2012).

To encounter the attacking pathogen including M. oryzae, rice triggers an array of sophisticated basal defense responses, which includes biosynthesis, signaling and cross-communication of various defense-related hormonal pathways, induction of oxidative burst and accumulation of antimicrobial substances (Nasir et al., 2018). Moreover, there is a growing belief that sugar molecules are also important for the establishment of successful defense against phytopathogens (Bolouri and Van, 2012). Besides, studies demonstrated that upon pathogen challenge plants including rice also fortify its cell wall which serves as a physical barrier to inhibit the penetration of the invading pathogens.

In the last two decades, remarkable progress has been made in understanding the role of phytohormones in rice plant defense against M. oryzae (Yang et al., 2013; Nasir et al., 2018). It has been demonstrated that phytohormones including ethylene (ET), jasmonic acid (JA) and salicylic acid (SA) are positive regulators for resistance against M. oryzae in rice, whereas abscisic acid, auxin and gibberellic acid render rice plants more susceptible to M. oryzae infection. As is evident that successful defense to M. oryzae in rice is dependent on the activation of ET-, JA- and SA-related pathways, the role of strigolactones (SLs) in regulating defense mechanism against devastating rice pathogens including that of M. oryzae remain elusive.

SLs for the first time was identified as a root exudate of cotton (Gossypium hirsutum L.) about 60 years ago (Cook et al., 1966) and, it has been found that SLs induce seed germination of parasitic plants (Orobanche, Phelipanche and Alectra) (Xie et al., 2010). Furthermore, years before, it was revealed that SLs as a host-derived signaling molecules are also involved in spore germination, and stimulation of hyphal branching of arbuscular mycorrhizal fungi, as well as in regulation of ectomycorrhizal fungi and gymnosperms interaction, resulting the symbiotic association between host plants and mycorrhizal fungi (Akiyama et al., 2005; Herrera-Martínez et al., 2014). Later on, it was found that SLs also serve as plant hormones, and regulate plant developmental and physiological processes, including seed germination, secondary growth, root development, branching and leaf senescence (Brewer et al., 2013). Besides, genetic studies have shown that SLs also positively mediate abiotic stress tolerance such as drought stress, salinity stress and nutrient stress in different plant species (Saeed et al., 2017).

In addition, to the roles of SLs in plant growth, development and abiotic stress resilience, more recently, genetic studies provided ample evidence that SLs also mediate defense against specific bacterial and fungal phytopathogens (Marzec, 2016). For instance, leaves of the tomato (Solanum lycopersicum) SL-deficient ccd8 mutants were highly vulnerable to infection caused by the fungi Botrytis cinerea and Alternaria alternate (Torres-Vera et al., 2014). Moreover, the Arabidopsis thaliana SL-biosynthetic, more axillary growth1 (max1), max3 (ortholog of dwarf17, d17 from rice), and max4 (ortholog of d10 from rice), and the SL-signaling max2 (ortholog of d3 from rice) mutants also showed enhanced susceptibility to the pathogen Rhodococcus fascians (Stes et al., 2015). Consistent with this, A. thaliana max2 mutant plants are also more vulnerable to phytopathogenic bacteria Pectobacterium carotovorum and Pseudomonas syringae than wild-type (WT) (Piisilä et al., 2015). In addition to tomato and A. thaliana, the positive role of SL in immunity also has been confirmed in moss (Physcomitrella patens), in such a way that SL-deficient ccd7 and ccd8 mutants of moss were more susceptible to Fusarium oxysporum, Sclerotinia sclerotiorum, and Irpex sp. infection than WT (Decker et al., 2017). On the contrary, genetic studies have shown that SL-biosynthetic pathway is not required for regulation of defense against F. oxysporum in pea (Pisum sativum L.) (Foo et al., 2016).

SLs biosynthetic pathway of rice consists of five main genes, named d27, d17, d10, and two Arabidopsis max1 orthologs (Os01g0700900 and Os01g0701400). d17, d10, d27, Os01g0700900 and Os01g0701400, coding for enzymes CCD7, CCD8, β-carotene isomerase, carlactone oxidase and orobanchol synthase respectively, function in β-carotene cleavage involving essential catalyzing steps, resulting biosynthesis of SLs (Saeed et al., 2017). In contrast, d14, d3 and d53 are well-known for their regulatory roles in SL-signaling. d14 and d3 are coding for receptor proteins namely α/β-hydrolase and F-box, respectively which perceive the presence of SLs and function as activators. On the contrary, d53 coding for a protein which shares predicted features with the class I Clp ATPase proteins and is known for repression of SLs signaling.

The purpose of the current study was to investigate whether SLs function in the regulation of rice defense against M. oryzae. To achieve this, we used well-defined rice SL-biosynthetic (d17) and -signaling (d14) defective mutants and the relevant WT rice plants. Results revealed that rice mutants defective in either SL-biosynthesis or -signaling exhibited increased susceptibility towards M. oryzae infection. Comparative transcriptome analysis revealed that the susceptibility was accompanied with the reduced expression of a large number of defense-associated genes including that of cell wall-, ET-, hydrogen peroxide (H2O2)-, and sugar/carbon synthesis-related genes. Accordingly, biochemical analysis showed clear reduction in H2O2 and soluble sugar contents in d17 and d14 mutants compared with that of WT in response to M. oryzae infection. Taken together, these results indicated that SLs promote biotic stress tolerance in rice by interacting cell wall-, ET-, H2O2- and sugar-associated genes/pathways.

Section snippets

Seeds and seedling growth

Seeds of rice d17 and d14 mutants and WT (Oryza sativa L. cv. Shiokari) were originally got from Junko Kyozuka group, Touhoku University, Japan. For getting seedlings, briefly, seeds of d17, d14 and WT were surface sterilized according to the method adapted by Tian et al. (2018). Next, germinating seeds were transplanted into 9 × 9 cm diameter pots (4 seedlings per pot) having 0.5 kg of sterilized soil and placed in the phytochamber. The temperature, photoperiod and relative humidity of the

SL-deficient and -signaling mutants reveal increased susceptibility to M. oryzae infection

To assess the possible role of SLs in defense against M. oryzae, the forth leaves of rice mutants that are defective in either SL biosynthesis (d17) or signaling (d14) and its corresponding WT rice were infected with a hemibiotrophic M. oryzae isolate, GUY11. Seven days later, the severity of disease was determined by evaluating the disease lesion size and number (Fig. 1). A significant increase in the susceptible-type lesion number was observed at 7 dpi in d17-and d14-infected plants compared

Discussion

Rice blast fungus, M. oryzae possesses a major threat to global food security, adversely affecting both rice crop yield and quality (Nasir et al., 2018). Given the importance of plant hormones in induction of host defense, tremendous progress has been made in the last two decades on understanding the role of these phytohormones in rice plant defense against M. oryzae (Yang et al., 2013; Nasir et al., 2018). In this context, it has been demonstrated that ET, JA and SA promotes disease resistance

Author contributions

CT and FN designed the experiments. FN, LT, CC, SS and LM performed the experiments and analyzed the data. FN, CT and YG wrote the manuscript.

Acknowledgments

This research work was financially supported by the Science Foundation of Chinese Academy of Sciences (XDA23070501, XDB15030103), the National Key Research and Development Program of China (2016YFC0501202), the Key Research Project of the Chinese Academy of Sciences (KFZD-SW-112), the National Natural Science Foundation of China (41571255), Cooperative Project between CAS and Jilin Province of China (2019SYHZ0039) the Science and Technology Development Project of Changchun City of China (18DY019

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