Abstract
During symbiosis, organisms use a range of metabolic and protein-based signals to communicate. Of these protein signals, one class is defined as ‘effectors’, i.e., small secreted proteins (SSPs) that cause phenotypical and physiological changes in another organism. To date, protein-based effectors have been described in aphids, nematodes, fungi and bacteria. Using RNA sequencing of Populus trichocarpa roots in mutualistic symbiosis with the ectomycorrhizal fungus Laccaria bicolor, we sought to determine if host plants also contain genes encoding effector-like proteins. We identified 417 plant-encoded putative SSPs that were significantly regulated during this interaction, including 161 SSPs specific to P. trichocarpa and 15 SSPs exhibiting expansion in Populus and closely related lineages. We demonstrate that a subset of these SSPs can enter L. bicolor hyphae, localize to the nucleus and affect hyphal growth and morphology. We conclude that plants encode proteins that appear to function as effector proteins that may regulate symbiotic associations.
Highlights
Symbiosis, defined as a durable interaction between two or more organisms, is a complex association that requires both physiological and morphological signaling, reception and alterations on the part of both organisms
Could plants encode similar “effector-like” proteins that, in turn, exert a level of influence on the activity of the symbiotic associates? Previous research supporting the influence of plants over microbial biology suggests that: (1) plants utilize a number of secondary metabolites to affect rhizospheric and endopsheric microbes[9], (2) general root exudates act as microbial chemoattractants[10], (3) plants produce strigolactones which act as signals in initiating mycorrhizal formation[11] and (4) flavonoids from plants function as antimicrobial compounds[12, 13]
It is generally understood that the discovery of small secreted proteins (SSPs) in newly sequenced plant genomes has been hampered by the lack of gene annotation for proteins smaller than 100 amino acids due to a high false positive discovery rate from computational prediction of small open reading frames (ORFs) and a lack of homology across plant genomes which constrains ab initio gene calling[22, 23]
Summary
Symbiosis, defined as a durable interaction between two or more organisms, is a complex association that requires both physiological and morphological signaling, reception and alterations on the part of both organisms. Many fungal lineages within the pathogenic/mutualistic continuum have evolved elaborate protein-based signals to influence their hosts in order to support their metabolic requirements during symbiosis[1]. These proteins, called effectors, are typically fungal strain- or species-specific, usually ≤250 amino acids in size, and carry a secretion signal motif that may be cysteine-rich. When viewed from the perspective of the fungal-encoded effector biology described to date, the outcome of symbiosis would appear to be heavily influenced by the colonizing fungus Is this true, or could plants encode similar “effector-like” proteins that, in turn, exert a level of influence on the activity of the symbiotic associates? The aim of this study was to determine if: (1) Populus encoded effector-like proteins are regulated during mutualistic symbiosis with the ectomycorrhizal fungus L. bicolor and (2) whether some of these proteins might be able to enter the hyphae of L. bicolor and affect the growth of the fungus
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