1 INTRODUCTION
In natural ecosystems, the dynamics of plant interactions with other
living organisms are complex. This is especially true for organisms that
rely on plants for shelter, nutrition, and reproduction, such as fungi
and insects (Chisholm, Coaker, Day, & Staskawicz, 2006; Panda & Khush,
1995). Although fungi and insects can provide some of the same useful
services in return, those that do not can be extremely harmful to plant
productivity. To mitigate the effects of biotic stress, plants employ a
diverse set of defense mechanisms including chemical, protein-derived
molecules, and physical barriers (Panda & Khush, 1995). Insects and
fungi must develop strategies in parallel to overcome these obstacles to
survive (Chisholm et al., 2006; Mello & Silva-Filho, 2002). The theory
of gene-for-gene coevolution has frequently been used to describe this
host plant genetic relationship to its arthropod and fungal communities
(Chisholm et al., 2006; Ehrlich & Raven, 1964; Mello & Silva-Filho,
2002; Thompson, 1988).
The gene-for-gene theory suggests a very simple dynamic for the genetic
interactions that occur between two species. A gene in the host plant
that is important in biotic relationships has a corresponding,
coevolving gene from a pathogen/insect which can lead to resistance or
susceptibility depending on the life history of the pathogen/insect
(Flor, 1971; Friesen, Meinhardt, & Faris, 2007). Much of the evidence
for these interactions has been found in crop systems where plant
species often have dominant, single-gene resistance to feeding
(Thompson, 1988). For example, there are over twenty different genes in
wheat (Triticum aestivum L.) that each confer resistance to the
Hessian fly, Mayetiola destructor (Thompson & Burdon, 1992).
Exposure of Hessian fly populations to these resistant varieties of
wheat created selection pressure that led to increased virulent gene
combinations in the pest (Gallun, 1977; Panda & Khush, 1995).
Similarly, in plant-fungal systems breeding for dominant resistance in
cereal crops resulted in new selective forces that increased virulent
gene frequencies in Puccinia spp. cereal rusts (X. M. Chen, 2005;
Pretorius, Singh, Wagoire, & Payne, 2000). This in turn can lead to an
evolutionary arms race between plants, insects, and fungi with the
continual development of mechanisms to overcome both genetic defenses
and virulent attacks (Bergelson, Kreitman, Stahl, & Tian, 2001;
Thompson & Burdon, 1992).
The relationships of host plant genetics and biotic association can also
be more complex than these crop breeding systems suggest, and they can
leave a lasting impact on genome structure (Lefebvre & Chèvre, 1995).
Host plant and biotic associations can lead to the expansion of gene
families responsible for the host plant response to biotic stress. For
example, the Kunitz protease inhibitors (KPIs) in Populus are
important in defense responses against insects by inhibition of
herbivore digestion (Haruta, Major, Christopher, Patton, & Constabel,
2001; Major & Constabel, 2008). The KPI gene family has greatly
expanded in response to insect attack through tandem duplication events
(Philippe, Ralph, Külheim, Jancsik, & Bohlmann, 2009). Similarly, plant
resistance (R ) genes, which are important in the defense response
of plants to fungal pathogen attack, have also expanded through tandem
and segmental duplication events due to biotic pressures (Hulbert, Webb,
Smith, & Sun, 2001; Leister, 2004). Analyzing how the genome is
structured in the host plant when it associates with fungi and insects
is important for studying these relationships and understanding the
complexities of their genetic interactions.
Given their rapid growth and vegetative reproduction, Populusspecies have become a focus for research into biofuel production making
them a valuable commercial crop (Meilan et al., 2002; Stanton, B. Neale,
& Li, 2010; Taylor, 2002). Populus has also become an important
genetic model for research into a wide variety of ecological and
adaptive traits (McKown et al., 2014), including interactions with the
biotic community (Crutsinger et al., 2014; Whitham et al., 2006). In
particular, interspecific hybrids of P. trichocarpa x P.
deltoides segregate for a wide variety of traits including resistance
to insect and fungal attack (G. Newcombe, 1998; George Newcombe &
Ostry, 2001b). Such hybrid family crosses can be used to identify
regions of the genome that are important in mediating biotic stress.
In this study, we investigated the genome composition of loci associated
with insect and fungal species in an interspecific Populusfamily. We surveyed insects and fungal pathogens in a P. deltoides
x P. trichocarpa pseudo-backcross family and used quantitative trait
locus (QTL) analysis and comparative genomics to address three main
questions: (1) Is there heritable, host genetic control of fungal and
insect species? (2) What protein domains and gene ontology terms are
enriched in the QTL intervals in the genomes of each Populusspecies? (3) What candidate genes in the intervals are unique to each
species when comparing the P. trichocarpa and P. deltoidesgenomes?