Molecular plant immunity against biotrophic, hemibiotrophic, and necrotrophic fungi

Abstract

Pathogenic fungi use diverse infection strategies to obtain nutrients from plants. Biotrophic fungi feed only on living plant tissue, whereas necrotrophic fungi kill host cells to extract nutrients. To prevent disease, plants need to distinguish between pathogens with different life cycles, as a successful defense against a biotroph, which often involves programmed cell-death around the site of infection, is not an appropriate response to some necrotrophs. Plants utilize a vast collection of extracellular and intracellular receptors to detect the signatures of pathogen attack. In turn, pathogens are under strong selection to mask or avoid certain receptor responses while enhancing or manipulating other receptor responses to promote virulence. In this review, we focus on the plant receptors involved in resistance responses to fungal pathogens and highlight, with examples, how the infection strategy of fungal pathogens can determine if recognition responses are effective at preventing disease.

Keywords: biotroph; necrotroph; plant immunity.

Figure 1. Extracellular and intracellular receptor proteins can promote disease resistance or susceptibility to fungal pathogens

Cell-surface receptors are embedded in the plasma-membrane while intracellular receptors are localized to the cytosol. The cell-surface receptors are grouped into subfamilies based on their extracellular domain/s. Lysin-motif receptor-like proteins and receptor-like kinases (LysM-RLP/RLKs) can detect chitin oligomers released from the fungal cell wall to activate defense responses that promote disease resistance against biotrophic, hemibiotrophic, and necrotrophic fungi without leading to plant cell death. Leucine-rich repeat (LRR) receptors can detect secreted proteins (effectors) from pathogenic fungi and mediate downstream immune signaling by forming receptor complexes with other LRR-RLKs (SOBIR1 and BAK1). Notably, the LRR-RLP/RLKs that detect effectors from necrotrophic fungi and promote disease resistance do not lead to plant cell death. Likewise, wall-associated kinase (WAK) receptor proteins activate responses that typically promote disease resistance. However, Snn1 from wheat detects a necrotrophic effector (Tox1) and triggers a cell-death response that supports the growth of the invading necrotroph. Inside the cell, intracellular receptors detect effectors and typically promote disease resistance by initiating a localized cell-death response that restricts the growth of biotrophic and hemibiotrophic fungi. However, multiple necrotrophic fungi use effectors to manipulate intracellular receptors into activating cell death, ultimately promoting disease susceptibility. Only the receptors discussed in this review are depicted in the figure.