Rapid change in host specificity in a field population of the biological control organism Pasteuria penetrans

Abstract

In biological control, populations of both the biological control agent and the pest have the potential to evolve and even to coevolve. This feature marks the most powerful and unpredictable aspect of biological control strategies. In particular, evolutionary change in host specificity of the biological control agent could increase or decrease its efficacy. Here, we tested for change in host specificity in a field population of the biological control organism Pasteuria penetrans . Pasteuria penetrans is an obligate parasite of the plant parasitic nematodes Meloidogyne spp., which are major agricultural pests. From 2013 through 2016, we collected yearly samples of P. penetrans from eight plots in a field infested with M. arenaria . Plots were planted either with peanut ( Arachis hypogaea ) or with a rotation of peanut and soybean ( Glycine max ). To detect temporal change in host specificity, we tested P. penetrans samples annually for their ability to attach to (and thereby infect) four clonal lines of M. arenaria . After controlling for temporal variation in parasite abundance, we found that P. penetrans from each of the eight plots showed temporal variation in their attachment specificity to the clonal host lines. The trajectories of change in host specificity were largely unique to each plot. This result suggests that local forces, at the level of individual plots, drive change in specificity. We hypothesize that coevolution with local M. arenaria hosts may be one such force. Lastly, we observed an overall reduction in attachment rate with samples from rotation plots relative to samples from peanut plots. This result may reflect lower abundance of P. penetrans under crop rotation, potentially due to suppressed density of host nematodes. As a whole, the results show local change in specificity on a yearly basis, consistent with evolution of a biological control organism in its ability to infect and suppress its target pest.

A diverse parasite pool can improve effectiveness of biological control constrained by genotype‐by‐genotype interactions

“…Collagen‐like proteins also play a critical role in P. penetrans attachment (Davies & Opperman, 2006 ), so the interaction effect for attachment that we observe in this study may reflect variation in compatibility between collagen‐like proteins of the P. penetrans sources and receptors, perhaps mucin‐like proteins, expressed on the cuticles of our host lines (Davies, 2009 ; Phani et al, 2018 ). Our results support the potential for coevolution of P. penetrans with M. arenaria and the maintenance of genetic variation via negative frequency‐dependent selection, wherein P. penetrans populations adapt to attach to locally common genotypes of M. arenaria (Liu et al, 2018 ).…”

“…penetrans with M. arenaria and the maintenance of genetic variation via negative frequency-dependent selection, wherein P. penetrans populations adapt to attach to locally common genotypes of M. arenaria (Liu et al, 2018).…”

“…The leading hypothesis for this variability is that infection depends on the specific interaction of host and parasite genotype (Channer & Gowen, 1992;Timper, 2009). A single isolate of P. penetrans can infect some Meloidogyne lines but not others (Stirling, 1985;Trudgill et al, 2000), with isolates differing in which lines they can infect (Liu et al, 2018;Timper, 2009). This hypothesis has support from the related bacterial parasite P. ramosa and its crustacean host Daphnia magna: the outcome of infection in this system rests upon a strong genotype-by-genotype interaction that manifests at the attachment stage (Carius et al, 2001;Duneau et al, 2011;Luijckx et al, 2011Luijckx et al, , 2013.…”

Plant Root-Exudates Recruit Hyperparasitic Bacteria of Phytonematodes by Altered Cuticle Aging: Implications for Biological Control Strategies

“…The role of root exudates, including the possible function of their containing phytohormones, has been shown to affect Pasteuria endospore attachment (Liu et al, 2017) and changes in host specificity between Pasteuria and the phytonematode community occur on a yearly basis (Liu et al, 2019); necessarily, this is the result of population regulatory outcomes from bottom-up control through the host plant, horizontal control of competition between phytonematodes, and topdown control by natural enemies (Van Der Putten et al, 2006). The importance of root-exudates in a plant's adaptive defense mechanism by maintaining a protective microbiome is an active area of investigation (Rolfe et al, 2019) and here, from a perspective of eco-evolutionary dynamics, we propose a model in which the role of the plant root exudates on the cuticular aging process is fundamental as they will be locked into a co-evolutionary arms race involving rhizosphere signaling directly between the host plant and its nematode parasite and indirectly by differentially affecting hyperparasitic recruitment.…”

The Fight against Plant-Parasitic Nematodes: Current Status of Bacterial and Fungal Biocontrol Agents

“…Liu et al explored the drivers of the specificity change of P. penetrans on M. arenaria in peanut plots and crop rotations with peanut and soybean. Their results show a rapid change in the host specificity of P. penetrans against M. arenaria , both in space and time, and they observed an overall reduction in the attachment rate with samples from rotation plots relative to samples from peanut plots, which may reflect the lower abundance of the bacterial antagonist under crop rotation, potentially due to suppressed density of host nematodes [ 43 ]. Ghahremani et al [ 31 ] studied the effects of B. firmus I-1582 on M. incognita and the root colonization of tomato and cucumber and noted that the bacterium degraded eggshells and colonized tomato roots more extensively than cucumber roots.…”