INTRODUCTION
A major challenge for modern agriculture is to implement sustainable
solutions ensuring food security by promoting crop health while
decreasing our reliance on agrochemicals
(Tilman, 2011).
Globalization and agricultural intensification have disrupted the
coevolutionary battle in which plants and pathogens engage in natural
ecosystems, generally favoring larger pathogen population sizes (i.e.,
more widespread and intense epidemics) and thus rapid evolution of
pathogen aggressiveness and infectivity
(Burdon & Thrall,
2008; Gladieux et al., 2015; Parker & Gilbert, 2004). Monocultures of
varieties bred for high yield and disease resistance are also vulnerable
to disease outbreaks, because they impose strong directional selection
on pathogens, and because mutants that can overcome resistance in one
individual plant can infect all plants in a field and hence quickly
spread (Hill, 2001;
Stukenbrock & McDonald, 2008; Zhan, Thrall, Papaïx, Xie, & Burdon,
2015). The literature in plant pathology provides many examples of
so-called boom-and-bust disease dynamics, in which newly deployed
resistant varieties are rapidly colonized by pathogen variants able to
overcome new resistance genes
(Brown, 1994; de
Vallavieille-Pope et al., 2012; Guérin, Gladieux, & Le Cam, 2007). In
contrast, in unmanaged, natural, ecosystems, pathogen prevalence is
generally lower, and disease epidemics more limited in time and
space (Burdon and
Thrall 2014). Long-term empirical studies and modeling work suggest that
ecological and environmental heterogeneity, with highly patchy and
variably diverse host plant populations, varying abiotic conditions and
the co-occurrence of closely related but distinct or
phylogenetically-distant plants can contribute to limit the burden of
disease in the wild
(Burdon & Thrall,
2008; Zhan et al., 2015). Metapopulation dynamics and frequency
dependent selection in heterogeneous environment create a mosaic of
local coevolutionary scenarios ranging from local adaptation to
maladaptation (Laine,
2007), depending on the biology of the system.
Traditional agrosystems are promising models for deriving new disease
management rules for modern agrosystems
(Chentoufi et al.,
2014; Sahri et al., 2014). Transfering knowledge gained from studies of
the mechanisms underlying the stability of plant-pathogen associations
in the wild (Burdon &
Thrall, 2008) is hindered by divergence in the structure and complexity
of unmanaged ecosystems and modern agrosystems caused by marked
differences in the impact of humans on the spatio-temporal distribution
of host diversity between the two types of systems. Unlike modern
agrosystems and modern crops, which have been engineered and intensely
selected to improve yield and quality under relatively low-stress
conditions, landraces and their agrosystems have been selected and
developed for their capacity to provide stable yields in specific
environmental conditions and under low-input agriculture. The value of
landraces as sources of genetic variation, or the value of traditional
agrosystems as models for re-engineering modern agrosystems, are
generally accepted
(Feuillet, Langridge,
& Waugh, 2008). Some studies have also been done at the field based
experimental level
(Zhan & McDonald,
2013). However, there has been remarkably little effort to investigate
causal links between the structure of genetic and phenotypic diversity
in crops and pathogens on the one hand and disease dynamics on the
other.
The traditional, centuries-old agrosystem of the Yuanyang terraces (YYT)
of flooded rice paddies (Yunnan, China) represents an outstanding model
system to investigate the factors that render plant agrosystems less
conducive to disease
(Liao et al., 2016).
More than 180 landraces, mostly indica rice, have been grown for
centuries in the Yuanyang terraces
(Gao, Mao, & Zhu,
2012; Jiao et al., 2012; Yang et al., 2017). The Yuanyang landraces are
famous for being little affected by diseases
(Sheng, 1990), such as
rice blast caused by Pyricularia oryzae (syn., Magnaporthe
oryzae ), which is an important rice disease worldwide
(R. Dean et al.,
2012).
Rice blast is widely spread on all ecotypes of rice and in different
ecological zones, where it has a massive socio-economic impact on human
populations (R. Dean
et al., 2012; Tharreau et al., 2009). Rice blast is caused by one out of
several host-specific lineages of P. oryzae(Gladieux et al.,
2018). The rice-specific lineage is subdivided in three clonal
(Gladieux et al.,
2018) and one recombining and genetically more diverse lineage mainly
distributed in Southeast Asia
(Gladieux et al.,
2018; Saleh, Milazzo, Adreit, Fournier, & Tharreay, 2014). Cross
inoculation experiments with globally distributed isolates pathogenic on
rice have revealed host specialization of P. oryzae to the main
groups of modern rice varieties
(Gallet et al., 2016;
Gladieux et al., 2018). In the traditional YYT agrosystem, local
adaptation to indica and japonica host ecotypes was also
observed, and was associated with major differences in basal and
effector-triggered immunity in the host
(Liao et al., 2016).
However, the coevolutionary interactions underlying the overall lower
disease burden observed in YYT, remains unknown.
In this study we addressed whether the lower disease pressure observed
on indica landraces, which represent 90 % of acreage in YYT,
could result from the elevated landrace diversity extant in YYT, which
hinders the emergence of P. oryzae populations specialized toindica landraces. We first analysed the population structure of
YYT rice landraces on the one hand and P. oryzae populations on
the other hand. We then used paired samples of P. oryzaepathogens and their plants of origin to address whether host and
pathogen populations were genetically co-structured in order to
establish if P. oryzae genotypes were specialized to their native
host genotypes.