1 INTRODUCTION
Understanding the mechanisms of co-occurring species interactions in
plant coexistence and community
assembly has been of great interest to ecologists for decades (Maron,
Hahn, Hajek, & Pearson, 2020; Tilman & Pacala, 1993). When one or more
species occur together and interact, plants may detect and recognize
their neighbors, potentially differentiating interspecific individuals
from conspecific individuals (Gruntman & Novoplansky, 2004), and even
intraspecifically between kin and
non-kin individuals (Dudley & File, 2007). Following
neighbor
detection and recognition, plants may adjust their growth and defense
strategies, altering plant coexistence and community assembly (Wang,
Kong, Wang, & Meiners, 2020).
The role of plant-plant interactions in regulating coexistence has been
a fundamental issue within ecology and evolution, focusing predominately
on interspecific and intraspecific competition
(Bennett,
Riibak, Tamme, Lewis, & Partel,
2016; Genung, Bailey, & Schweitzer, 2012; Yamawo & Mukai, 2020). In
recent decades, this issue research has expanded to include both kin
recognition and allelopathy
(Bilas, Bretman, & Bennett, 2020;
Kong et al., 2018). Kin recognition may allow plants to optimize
competitive strategies, resulting in less intraspecific competition and
more cooperation among plants, maximizing stand performance (Bilas,
Bretman, & Bennett, 2020; Dudley, Murphy, & File, 2013). Kin
recognition in crop cultivars may also be exploited to improve crop
yields (Anten, & Chen, 2021; Murphy, Swanton, van Acker, & Dudley,
2017). In contrast to the altruism of intraspecific kin recognition,
allelopathy is an interference mechanism in which plants produce and
release allelochemicals exerting a mostly negative effect on
interspecific or intraspecific neighbors. Such allelopathic
interferences can have profound effects on the performance of
neighboring plants and alter local plant coexistence (Meiners, Kong,
Ladwig, Pisula, & Lang, 2012; Zhang, Liu, Yuan, Weber, & van Kleunen,
2020). Noteworthily, different from competition for taking up shared
resources, allelopathy is a chemical strategy in the defense of plant
against competing neighbors, which results from the allelochemicals
produced and released from plants themselves (Macías, Mejías, &
Molinillo, 2019).
Both kin recognition and allelopathy have been investigated extensively
in natural and managed ecosystems (Anten, & Chen, 2021; Inderjit,
Wardle, Karban, & Callaway, 2011; Macías, Mejías, & Molinillo, 2019;
Serra, Shanmuganathan, & Becker, 2021). However, kin recognition and
allelopathic interference are usually studied separately, with no
attention to their
potential
linkage. Plants often grow in mixtures of kin, non-kin conspecifics, and
individuals from different species, and thus kin recognition and
interspecific allelopathic interference may often occur simultaneously.
Accordingly, kin recognition may interact with allelopathic interference
within a heterogenous community context.
Ultimately,
understanding the
interactions between kin recognition
and allelopathic interference in diverse natural systems will depend on
initial efforts from simplified agroecosystems.
Crop plants have coexisted with weeds in agroecosystems for thousands of
years and can act as models for addressing eco-evolutionary dynamics in
plant coexistence (Baucom, & Holt, 2009). Weeds pose an important
biological constraint to crop productivity while only a few crop
cultivars are very competitive against weeds. However, the
weed-suppressive effects have not been fully explained by considering
just the physical characteristics of being strong in competition for
resources (Bastiaans, Kropff, Kempuchetty, Rajan, & Migo, 1997;
Olofsdotter, Navarez, Rebulanan, & Streibig, 1999). Subsequent studies
have shown the participation of allelopathy. In particular, allelopathic
crop cultivars can detect the presence of weeds and respond by
increasing allelochemicals to inhibit weeds, maximizing their own growth
(Kato-Noguchi, 2011; Kong et al., 2018; Kong, Li, Hu, Xu, & Wang,
2006). Therefore, crop-weed interactions are not only of fundamental
ecological interest, but also exceedingly important from an applied
perspective in sustainable agriculture.
Rice
(O ryza
sativa ) is one of the principal food crops in the world, containing
both allelopathic and non-allelopathic cultivars. Allelopathic rice
cultivars can produce and release allelochemicals to inhibit the growth
and establishment of paddy weeds, acting as an efficient component of
integrated weed management (Kong,
Hu, Wang, & Wu,
2008; Patni et al., 2018; Serra,
Shanmuganathan, & Becker, 2021). Recent studies have shown kin
recognition in rice cultivars (Fang
et al., 2013) and allelopathic rice cultivars with the ability for kin
recognition can alter root behavior and biomass allocation, increasing
grain yields (Yang, Li, Xu, & Kong, 2018). Therefore, allelopathic rice
interference with paddy weeds represents a well-characterized model
system to understand the combined roles of kin recognition and
interspecific allelopathy in plant-plant interactions.
There is a wealth of information on allelopathic rice interference with
paddy weeds under field situations and controlled conditions (Gealy,
Rohlla, & Boykin, 2019;
Kato-Noguchi,
2011; Kong, Hu, Wang, & Wu, 2008; Li, Zhao, & Kong, 2020). However,
when it comes to the role of kin recognition in allelopathic rice
interference with paddy weeds, there is a lack of data. Such information
is critical for understanding the consequences and mechanisms of
plant coexistence in the given
ecosystem. In this study, we identify the
potential
linkage between kin recognition and allelopathic interference in a rice
paddy model system, to test two specific
hypotheses (1) whether
kin recognition can alter the
consequences of interspecific allelopathic interference, and (2) whether
relatedness allows allelopathic plants to discriminate between
neighboring collaborators (kin) and competitors by altering biochemical
plasticity and then adjust their growth, competitiveness, and chemical
defense. To do this, we examined
the effects of allelopathic rice cultivars with the ability for kin
recognition from two sets of indica-inbred and indica-hybrid rice lines
against paddy weeds in field and controlled conditions. Furthermore, we
addressed potential mechanisms through documenting changes in root
behavior, allelochemical production, associated soil microbial
communities, and the carbon and nitrogen partitioning of weeds.
Together, these efforts provide a thorough assessment of the
contribution of kin recognition to
allelopathic interference, and its implications for plant coexistence
and community assembly.