Mitochondrial dynamics and mitophagy are necessary for proper invasive growth in rice blast.

Yanjun Kou,Jiehua Qiu,Fan Yang,Yizhen Deng,Yazhou Shu,Yunlong He,Naweed I Naqvi

doi:10.1111/mpp.12822

Abstract

Summary Magnaporthe oryzae causes blast disease, which is one of the most devastating infections in rice and several important cereal crops. Magnaporthe oryzae needs to coordinate gene regulation, morphological changes, nutrient acquisition and host evasion in order to invade and proliferate within the plant tissues. Thus far, the molecular mechanisms underlying the regulation of invasive growth in planta have remained largely unknown. We identified a precise filamentous‐punctate‐filamentous cycle in mitochondrial morphology during Magnaporthe–rice interaction. Interestingly, disruption of such mitochondrial dynamics by deletion of genes regulating either the mitochondrial fusion (MoFzo1) or fission (MoDnm1) machinery, or inhibition of mitochondrial fission using Mdivi‐1 caused significant reduction in M. oryzae pathogenicity. Furthermore, exogenous carbon source(s) but not antioxidant treatment delayed such mitochondrial dynamics/transition during invasive growth. In contrast, carbon starvation induced the breakdown of the mitochondrial network and led to more punctate mitochondria in vitro. Such nutrient‐based regulation of organellar dynamics preceded MoAtg24‐mediated mitophagy, which was found to be essential for proper biotrophic development and invasive growth in planta. We propose that precise mitochondrial dynamics and mitophagy occur during the transition from biotrophy to necrotrophy and are required for proper induction and establishment of the blast disease in rice.

Highlights

Mitochondria, the semi-autonomous double-membrane bound organelles, generate most of the adenosine triphosphate (ATP) for diverse cellular functions and are involved in various physiological processes including lipid metabolism, redox signalling, calciumand iron-homeostasis, and programmed cell death (Zemirli & Morel, 2018, Nunnari &Suomalainen, 2012)
Our study demonstrates that tightly controlled mitochondrial dynamics and mitophagy are required for proper invasive growth during establishment of the blast disease in rice
Mitochondrial morphology was examined at the following three time points post inoculation: 30 hpi when the fungus successfully penetrated the rice epidermis, 48 hpi when most of invasive hyphae spread into the neighbouring rice cells and necrotrophy starts to occur, and 72 hpi when necrotrophy/lesion formation could be observed

Summary

Introduction

Mitochondria, the semi-autonomous double-membrane bound organelles, generate most of the adenosine triphosphate (ATP) for diverse cellular functions and are involved in various physiological processes including lipid metabolism, redox signalling, calciumand iron-homeostasis, and programmed cell death (Zemirli & Morel, 2018, Nunnari &Suomalainen, 2012). The mitochondrial shape is dynamic and depends on the balance between two opposing processes, fusion and fission, which occur continuously during the growth cycle (Westermann, 2010). Maintaining the mitochondrial morphology in steady state by the balance of fusion and fission activities is critical for living cells. When this equilibrium is broken, mitochondrial shape and dynamics are disturbed leading to important physiological consequences including increased cellular stress and various diseases

Results

Discussion

Conclusion