Mixed Disease Phenotype Results
Despite the significant trend of the number of R genes increasing with
CMI, leaf rust severity, leaf rust response, and stem rust severity did
not significantly vary in the common gardens. These three traits are
different phenotypic metrics to assess a specialist fungal pathogen,Puccinia silphii , commonly known as Silphium rust. These
results are consistent with results from common gardens that found that
eastern populations of S. integrifolium were not, on average,
more resistant to Silphium rust (Cassetta et al., 2023). One
possible explanation for why resistance to Silphium rust was not
associated with variable R gene counts may lie in the concept of the
‘disease triangle’ reviewed by Velásquez et al., 2019. The clones in
this study were placed in environments where S. integrifoliumpathogens were present, and experienced conditions that would be ideal
for pathogenic growth: warm and wet. Even with effective immunity
represented by the R genes sequenced in the plant populations, the level
of resistance conferred by the resistance genes might have been obscured
by the pathogen spread. Disease resistance in these wild populations is
highly likely to be quantitative, meaning that resistance is not an
all-or-nothing response, but rather a distribution of potential
responses ranging from minor to major (French et al., 2016). Further
studies of the wild populations with sequenced R genes, with controlled
inoculations of plants with pathogens, would elucidate associations
between R genes that may confer various levels of response to pathogens.
Further, the evolutionary dynamics of R genes may be muddled by
seemingly competing forces of selection, with “arms race” dynamics
expected to generate gradients in total host resistance, while
oscillatory “red-queen” dynamics may not (Bergelson et al., 2002). It
is possible, for example, that local co-evolution of S.
integrifolium and Silphium rust has resulted in adaptation of
the rust to its local host population, rather than variation in overall
resistance. This red-queen dynamic is supported by observations from
common gardens distributed along the gradient that showed much greater
virulence of Silphium rust on their populations from their local
region than from other regions (Cassetta et al. 2023). In the case ofSilphium rust, R gene identity may be more important than R gene
diversity.
We did observe that resistance allele diversity was associated with
suppression of leaf blotch (Fig. 6d). Our result affirms observations of
a previous common garden study that found that eastern populations ofS. integrifolium were more resistant to Silphium blotch,
as well as to clear vein virus (Cassetta et al. 2023). These results are
consistent with expectations of greater diversity of resistance alleles
contributing to greater resistance to pathogens, and are qualitatively
consistent with arms-race-type dynamics. In S. integrifolium ,
leaf blotch is caused by the generalist fungal pathogenColletotrichum dematium (Cybernome; Farr 1989), as well as its
more specialized congener, Colletotrichum silphii Davis (Horst
2008). It is possible that arms race dynamics are more likely between
hosts and generalist pathogens such as leaf blotch, while specialist
pathogens such as the Silphium rust are more likely to generate
red-queen dynamics.
We note that the observed relationship between resistance allele
diversity and resistance to blotch may be spurious, as other heritable
factors that covary with rainfall might contribute to disease
resistance, such as plant secondary chemicals. We note, however, that
insect herbivory may be an indicator of such overall resistance, and we
did not observe any relationship between R gene diversity and insect
leaf herbivory. This result is consistent with R genes predominantly
acting as pathogen effector receptors, and not targeted toward
resistance for insects (Chovelon et al., 2021).
A BROADER PATTERN OF R GENE EVOLUTION