Abstract
Interactions between plant-parasitic nematodes and their hosts are mediated by effectors, i.e. secreted proteins that manipulate the plant to the benefit of the pathogen. To understand the role of effectors in host adaptation in nematodes, we analysed the transcriptome of Heterodera sacchari, a cyst nematode parasite of rice (Oryza sativa) and sugarcane (Saccharum officinarum). A multi-gene phylogenetic analysis showed that H.sacchari and the cereal cyst nematode Heterodera avenae share a common evolutionary origin and that they evolved to parasitise monocot plants from a common dicot-parasitic ancestor. We compared the effector repertoires of H.sacchari with those of the dicot parasites Heteroderaglycines and Globodera rostochiensis to understand the consequences of this transition. While, in general, effector repertoires are similar between the species, comparing effectors and non-effectors of H.sacchari and G.rostochiensis shows that effectors have accumulated more mutations than non-effectors. Although most effectors show conserved spatiotemporal expression profiles and likely function, some H.sacchari effectors are adapted to monocots. This is exemplified by the plant-peptide hormone mimics, the CLAVATA3/EMBRYO SURROUNDING REGION-like (CLE) effectors. Peptide hormones encoded by H.sacchari CLE effectors are more similar to those from rice than those from other plants, or those from other plant-parasitic nematodes. We experimentally validated the functional significance of these observations by demonstrating that CLE peptides encoded by H.sacchari induce a short root phenotype in rice, whereas those from a related dicot parasite do not. These data provide a functional example of effector evolution that co-occurred with the transition from a dicot-parasitic to a monocot-parasitic lifestyle.
Highlights
Plant-parasitic nematodes cause damage to world agriculture valued at approximately $80 billion each year (Nicol et al, 2011; Jones et al, 2013)
In general, effector repertoires are similar between the species, comparing effectors and non-effectors of H. sacchari and G. rostochiensis shows that effectors have accumulated more mutations than non-effectors
The CLAVATA3/EMBRYO SURROUNDING REGION-like (CLE) proteins are modified by plant cell machinery in a manner similar to that of the endogenous proteins and the CLE peptides themselves subsequently interact with the CLAVATA2 receptor protein, which is required for nematode parasitism (Replogle et al, 2011; Replogle et al, 2013)
Summary
Plant-parasitic nematodes cause damage to world agriculture valued at approximately $80 billion each year (Nicol et al, 2011; Jones et al, 2013). The first effector identified from any plant-parasitic nematode was a beta 1,4 endoglucanase (cellulase) from the potato cyst nematode Globodera rostochiensis (Smant et al, 1998) and a range of cell wall degrading and modifying proteins have subsequently been identified as cyst nematode effectors including pectate lyase (Popeijus et al, 2000), GHF43 Arabinase (Cotton et al, 2014), GH53 Arabinogalactan endo- 1,4 beta galactosidase (Vanholme et al, 2009), expansins (Qin et al, 2004) and proteins encoding carbohydrate binding domains (Hewezi et al, 2008) All of these genes, as well as others encoding chorismate mutase (Jones et al, 2003) and proteins potentially involved in vitamin biosynthesis (Craig et al, 2008), have been acquired by horizontal gene transfer from bacteria (reviewed in Kikuchi et al, 2017). We show that in general the effectors have diversified in sequence more than non-effectors when compared to their most similar homologue in a dicotparasite, and that while some effectors show conserved expression profiles and likely function, specific aspects of the effector repertoire of H. sacchari appear to be adapted to monocots
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