Suppression of Plant Immunity by Fungal Chitinase-like Effectors

Abstract

Crop diseases caused by fungi constitute one of the most important problems in agriculture, posing a serious threat to food security [1]. To establish infection, phytopathogens interfere with plant immune responses [2, 3]. However, strategies to promote virulence employed by fungal pathogens, especially non-model organisms, remain elusive [4], mainly because fungi are more complex and difficult to study when compared to the better-characterized bacterial pathogens. Equally incomplete is our understanding of the birth of microbial virulence effectors. Here, we show that the cacao pathogen Moniliophthora perniciosa evolved an enzymatically inactive chitinase (MpChi) that functions as a putative pathogenicity factor. MpChi is among the most highly expressed fungal genes during the biotrophic interaction with cacao and encodes a chitinase with mutations that abolish its enzymatic activity. Despite the lack of chitinolytic activity, MpChi retains substrate binding specificity and prevents chitin-triggered immunity by sequestering immunogenic chitin fragments. Remarkably, its sister species M. roreri encodes a second non-orthologous catalytically impaired chitinase with equivalent function. Thus, a class of conserved enzymes independently evolved as putative virulence factors in these fungi. In addition to unveiling a strategy of host immune suppression by fungal pathogens, our results demonstrate that the neofunctionalization of enzymes may be an evolutionary pathway for the rise of new virulence factors in fungi. We anticipate that analogous strategies are likely employed by other pathogens.

Rapid evolution in plant–microbe interactions – a molecular genomics perspective

“…An extension of this concept is the evolution of catalytically inactive variants of secreted proteins. Examples include the functional conversion of a glutathione synthetase in a plant-parasitic nematode (Lilley et al, 2018), enzymatically inactive fungal chitinases that sequester immunogenic chitin fragments (Fiorin et al, 2018), or the large family of catalytically inactive RNase-like effector proteins in cereal powdery mildews (Pennington et al, 2019).…”

Secretome Analysis of the Banana Fusarium Wilt Fungi Foc R1 and Foc TR4 Reveals a New Effector OASTL Required for Full Pathogenicity of Foc TR4 in Banana

“…Chitin and β-glucan, both of which are fungal cell wall polysaccharides, also serve as pathogen-associated molecular patterns (PAMPs) in plant. Pathogen-secreted chitinases with only binding ability prevent chitin-triggered immunity by sequestering chitin fragments [ 24 ], while the roles of 1,3-beta-glucosidases secreted by plant pathogens are largely unknown [ 25 ]. The functions of glucan 1,3-beta-glucosidases are well characterized in mammalian pathogens, allowing fungi to avoid host immune stimulation by β-glucan through secretion of endo-1,3-beta-glucosidase to remove any exposed β-glucan polysaccharide [ 26 ].…”

The pathogen Moniliophthora perniciosa promotes differential proteomic modulation of cacao genotypes with contrasting resistance to witches´ broom disease.

“…Transgenic plants expressing chitinases increases its resistance against fungus and other pathogens, once chitin fragments are important pathogenassociated molecular pattern (PAMP), which recognition by hosts results in activation of defense signaling pathways [57]. However, recently Fiorin and colleagues (2018) [58], observed that M. perniciosa evolved an enzymatically inactive chitinase (MpChi) that binds with chitin immunogenic fragments, therefore prevents chitin-triggered immunity, evidencing a strategy of immune suppression of the host response by the pathogen. Moreover, PAMPs are expressed during biotrophic development and recent studies showed that Cerato-platanin, a PAMP from M. perniciosa, might bind chitin in a high affinity way, leading to an eliciting of plant immune system by fungal chitin released fragments [59,60].…”