Melanin Promotes Spore Production in the Rice Blast Fungus Magnaporthe oryzae.

Pengyun Huang,Huijuan Cao,Jing Wang,Siyi Zhu,Yan Li,Jianping Lu,Xiaohong Liu,Fu-Cheng Lin,Qing Wang

doi:10.3389/fmicb.2022.843838

Abstract

The rice blast pathogen, Magnaporthe oryzae, spreads through spores and invades rice through appressoria. Melanin is necessary for an appressorium to penetrate plant cells, but there are many unknown aspects of its role in fungal conidiation. In this study, we confirmed that melanin promotes spore production in M. oryzae, and that this effect is related to the background melanin content of wild-type strains. In the wild-type 70-15 strain with low melanin content of aerial hyphae, increased melanin synthesis promoted sporulation. In contrast, increased melanin synthesis in the wild-type Guy11 strain, which has higher melanin content, did not promote sporulation. The transcription factor Cnf1 (conidial production negative regulatory factor 1), which negatively regulates melanin synthesis, has opposite effects in conidiophore differentiation of Guy11 and 70-15. Deletion of CNF1 did not abolish the defects of Δcos1 and Δhox2 (where COS1/conidiophore stalk-less 1 or HOX2/homeodomain protein 2 was deleted) in conidiation, while increased the conidiation of Δgcc1 and Δgcf3 (where GCC1/growth, conidiation and cell wall regulatory factor 1, or GCF3/growth and conidiation regulatory factor 3 was deleted). Pig1 (pigment of Magnaporthe 1) regulates the melanin synthesis of hyphae but not of conidiophores, spores, or appressoria. Deletion of the same gene in different wild-type strains can lead to different phenotypes, partly because of differences in melanin content between fungal strains. Overall, this study reveals the functional diversity and complexity of melanin in different M. oryzae strains.

Highlights

Rice blast, Magnaporthe oryzae, is a plant pathogen that seriously harms the production of rice, wheat, and other gramineous crops all over the world (Dean et al, 2012)
When cultured on complete medium (CM), pig1Guy11, cnf1Guy11, and cnf1 pig1Guy11 were brownish green on their sporeforming aerial mycelium sides, different from the black displayed by the wild-type Guy11. pig1Guy11 and cnf1 pig1Guy11 were yellow to brown on their substrate mycelium sides, while Guy11 and cnf1Guy11 were black (Figure 1A). cnf170-15 and cnf1 pig170-15 were gray black, darker than that of the wildtype 70-15
We measured melanin contents in the spore-forming aerial mycelia of pig1, cnf1, and cnf1 pig1 derived from both wild-type strains Guy11 and 70-15 (Figures 1B,C)

Summary

INTRODUCTION

Magnaporthe oryzae (synonym Pyricularia oryzae), is a plant pathogen that seriously harms the production of rice, wheat, and other gramineous crops all over the world (Dean et al, 2012). 1,8-dihydroxynaphthalene (DHN)melanin is a virulence factor for many pathogenic fungi, such as Gaeumannomyces graminis, Colletotrichum lagenarium, and Pestalotiopsis fici (Kubo et al, 1982; Money et al, 1998; Jacobson, 2000; Zhang et al, 2019) Some chemical fungicides, such as tricyclazole, pyroquilon, phthalide, and carpropamid have been used to prevent rice blast disease (Woloshuk et al, 1983). Deleting melanin synthesis genes has separate and individual effects on spore production in different strains (Zhu et al, 2021). In the M. oryzae strain 70-15 with lower melanin content, increased melanin content promotes fungal conidiation, while in strain Guy, which always has high melanin content, continuing to increase melanin content no longer promotes conidiation

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DATA AVAILABILITY STATEMENT