Pyricularia oryzae: Lab star and field scourge

Abstract

Pyricularia oryzae (syn. Magnaporthe oryzae), is a filamentous ascomycete that causes a major disease called blast on cereal crops, as well as on a wide variety of wild and cultivated grasses. Blast diseases have a tremendous impact worldwide particularly on rice and on wheat, where the disease emerged in South America in the 1980s, before spreading to Asia and Africa. Its economic importance, coupled with its amenability to molecular and genetic manipulation, have inspired extensive research efforts aiming at understanding its biology and evolution. In the past 40 years, this plant-pathogenic fungus has emerged as a major model in molecular plant-microbe interactions. In this review, we focus on the clarification of the taxonomy and genetic structure of the species and its host range determinants. We also discuss recent molecular studies deciphering its lifecycle.

Taxonomy: Kingdom: Fungi, phylum: Ascomycota, sub-phylum: Pezizomycotina, class: Sordariomycetes, order: Magnaporthales, family: Pyriculariaceae, genus: Pyricularia.

Host range: P. oryzae has the ability to infect a wide range of Poaceae. It is structured into different host-specialized lineages that are each associated with a few host plant genera. The fungus is best known to cause tremendous damage to rice crops, but it can also attack other economically important crops such as wheat, maize, barley, and finger millet.

Disease symptoms: P. oryzae can cause necrotic lesions or bleaching on all aerial parts of its host plants, including leaf blades, sheaths, and inflorescences (panicles, spikes, and seeds). Characteristic symptoms on leaves are diamond-shaped silver lesions that often have a brown margin and whose appearance is influenced by numerous factors such as the plant genotype and environmental conditions. USEFUL WEBSITES Resources URL Genomic data repositories http://genome.jouy.inra.fr/gemo/ Genomic data repositories http://openriceblast.org/ Genomic data repositories http://openwheatblast.net/ Genome browser for fungi (including P. oryzae) http://fungi.ensembl.org/index.html Comparative genomics database https://mycocosm.jgi.doe.gov/mycocosm/home T-DNA mutant database http://atmt.snu.kr/ T-DNA mutant database http://www.phi-base.org/ SNP and expression data https://fungidb.org/fungidb/app/.

Keywords: Magnaporthe oryzae; Pyricularia oryzae; blast disease; disease cycle; fungus; genome; pathogen.

FIGURE 1

Pyricularia oryzae populations structure and their hosts of origin. Schematic distribution of P. oryzae main lineages and their hosts of origin. The host taxonomic tribe is indicated in brackets.

FIGURE 2

Pyricularia oryzae genome data. (a) Schematic representation of P. oryzae chromosomes (Ch.) and their estimated size in megabases (Mb) The approximate position of centromere according to Yadav et al. (2019) is represented by the dark blue shape. (b) Relative genome content of P. oryzae reference isolate 70–15 (Dean et al., 2005).

FIGURE 3

The cellular biology of Pyricularia oryzae life cycle. When an asexual spore (called a conidium) lands on the surface of a plant leaf it secretes mucilage to adhere to the leaf surface within minutes (Hamer et al., 1988) (panel 1). Following adhesion, the three‐celled conidium forms a germ tube from its apex. Shortly after, the tip of the hypha hooks and swells to form a specialized structure called an appressorium. During maturation, the appressorium is wrapped in a thick layer of melanin that retains glycerol, which translates into water uptake and a massive increase of turgor pressure (up to 8 MPa) (panel 2). Rearrangements of the cytoskeleton target the pressure towards the base of the appressorium, which breaks the leaf cuticle and penetrates the host epidermis cell about 20 h after adhesion of the conidium (Ryder et al., 2013). The penetration peg then differentiates into a primary invasive hypha that progresses in the host cytoplasm surrounded by the extra‐invasive hyphal matrix (EIHMx) and the extra‐invasive hyphal membrane (EIHM) (panel 3) (Oliveira‐Garcia et al., 2023). At the tip of the filamentous invasive hypha a specific dome‐shaped structure called the biotrophic interfacial complex (BIC) is formed (Khang et al., ; Valent & Khang, 2010). The BIC is a mainly plant‐derived structure that seems to be critical for the secretion of effector proteins in the host cytoplasm while apoplastic effectors localized in the EIHMx are secreted via the classic secretory pathway (Giraldo et al., 2013). The development of intracellular hyphae then switches to form bulbus hyphae that invade the host cell while still being enclosed by the EIHM (panel 4). The tip‐BIC is moved to the side of the first bulbus hypha, which correlates with a switch in vesicle content (Oliveira‐Garcia et al., 2023). Around 30 h post‐infection, the EIHM ruptures leading to the spill of the EIHMx content in the cytoplasm, and the vacuole of the host cell shrinks (Jones et al., 2021). The vacuole then disrupts, which correlates with the death of the primary infected cell. The invasive hyphae continue to grow in the dead cell, becoming more filamentous and getting closer to the cell wall (Jones et al., 2021). Movement from cell to cell is mediated by the localization of hyphae to pit fields, the hyphae then undergo a constriction to go through the pit fields and invade the next cell; these structures are called transpressoria (Cruz‐Mireles et al., ; Sakulkoo et al., 2018) (panel 5). The invasion of adjacent cells follows a similar pattern to the infection of the primary cell with first a filamentous hypha emerging from the pit field, capped by a BIC and surrounded by the EIHM. The cycle of biotrophic invasion and cell death continues until around 4 days after the start of the infection, when the fungus undergoes another switch in development with necrotrophic growth characterized by the development of apoplastic filamentous hyphae. This coincides with the appearance of symptoms in the form of diamond‐shaped silver lesions. Asexual reproduction is initiated with the formation of conidiophores outside the leaf tissues initiating a new cycle of infection (Lau & Hamer, 1998) (panel 6).