4 DISCUSSION
Intraspecific genetic variation can have important ecological
consequences for interspecific interactions (Ehlers, David, Damgaard, &
Lenormand, 2016; Fridley & Grime, 2010; Genung,
Bailey, & Schweitzer, 2012).
Kin
recognition and allelopathic interference are important mediators of
interspecific or intraspecific interactions among plants (Bilas,
Bretman, & Bennett, 2020; Dudley, Murphy, & File, 2013; Kong et al.,
2018; Wang, Kong, Wang, & Meiners, 2020). From a model system of
allelopathic
rice interference with paddy weeds, this study presents the first
evidence that intraspecific kin recognition may have consequences for
interspecific allelopathic interference. In particular,
this study makes the case for a
novel mechanism: that reductions in the costs associated with
intraspecific interactions with kin allow increased interspecific
allelopathic inhibition of co-occurring
weeds.
The direct evidence and mechanisms were that, when grown with closely
related cultivars, there was (1) increased
weed inhibition, maintaining rice
grain biomass; (2) reduced production of rice allelochemicals, lowering
defense cost; (3) altered root placement towards weeds, reconciling
niche partitioning and competitive ability; (4) generated similar soil
microbial community structure; and (5) altered carbon and nitrogen
partitioning of weed species.
A plant may interfere with
neighboring plant growth and establishment directly through competition,
allelopathy, or both. In allelopathic rice against paddy weeds, the
weed-suppressive effect is a combination of allelochemical action and
interspecific competition (Kong, Hu, Wang, & Wu, 2008). Allelopathy and
competition are well known to regulate inter- and intra-specific
interactions and community assembly (Fernandez et al., 2016; Inderjit,
Wardle, Karban, & Callaway, 2011; Xia, Kong, Chen, Wang, & Wang,
2016). An increasing number of studies have shown that kin recognition
in plants can also alter the outcome of intraspecific and interspecific
competition and determine species coexistence (Dudley, Murphy, & File,
2013; Ehlers, David, Damgaard, & Lenormand, 2016; Yamawo & Mukai,
2020). In some plant communities, there is a reciprocal relationship
between competition and intraspecific trait variation (Bennett, Riibak,
Tamme, Lewis, & Partel, 2016). In particular, intraspecific genetic
relatedness may be more important than variation among species in
determining species coexistence (Ehlers, David, Damgaard, & Lenormand,
2016; Fridley & Grime, 2010).
These studies have revealed the
linkage between kin recognition and competition in plant coexistence and
community assembly. In the current study, we extend this observation to
both competition and allelopathy.
Intraspecific genetic relatedness in rice enhanced root intrusive
behavior towards paddy weeds, affecting competition and allelopathy.
Furthermore, kin recognition reduced the production of allelochemicals
in rice cultivar mixtures with closely related cultivars. Root
inhibition of paddy weeds mainly result from allelochemicals and
intrusive roots of allelopathic rice cultivars generating avoidance
patterns in weed roots (Yang & Kong, 2017). This study highlights that
kin mixtures result in stronger root inhibition and avoidance growth of
paddy weeds than non-kin cultivar mixtures, even with reduced production
of allelochemicals. Therefore,
weed inhibition appears to be
generated by targeted kin recognition through altered root placement,
reconciling niche partitioning and
competitive ability, rather than an overall
upregulation of allelochemicals.
Allelopathic rice cultivars produce and release allelochemicals against
paddy weeds. However, the production of allelochemicals must also incur
a defense cost, subsequently generating a trade-off between growth and
defense (Meiners, Kong, Ladwig, Pisula, & Lang, 2012). A plant can
change its defensive strategy based on the identity of its neighbors
(Broz et al., 2010; Metlen, Aschehoug, & Callaway, 2009; Pierik,
Mommer, & Voesenek, 2013). The production of allelochemicals also
depends on co-occurring plant species (Kong et al., 2018; Ormeno,
Fernandez, & Mevy, 2007; Xia, Kong, Chen, Wang, & Wang, 2016). The
production of allelochemicals may be decreased in the presence of a
“good” neighbor like the kin cultivars in this study, representing a
benefit to the allelopathic plant while maintaining a reduced cost to
the kin.
Plant neighbor recognition and allelochemical responses have been well
documented between species (Kong et al., 2018;Lankau & Strauss, 2007;
Pierik, Mommer, & Voesenek, 2013), but less is known about
intraspecific kin and non-kin interactions. Several studies have shown
that relatedness of neighboring plants mediates the expression of
indirect defense traits (Karban, Shiojiri, Ishizaki, Wetzel, & Evans,
2013; Kalske, Shiojiri, Uesugi, Sakata, & Kessler, 2019; Yamawo, 2015).
However, these studies have been primarily in the context of
herbivore-induced defenses rather than direct plant-plant interactions.
Data generated in this study revealed that kin recognition also affect
chemical defenses in plant-plant interactions, reducing the production
of allelochemicals in the presence of close relatives, shifting
allocation from defense into growth.
Plants differentiate their neighbors based on genetic relatedness and
alter functional traits in response to intraspecific competition
(Donohue, 2003; Dudley, Murphy, & File, 2013). Functional trait
responses can result in kin facilitation and cooperative behavior
(Ehlers, David, Damgaard, & Lenormand, 2016). Functional changes in
response to the presence of kin particularly alter patterns of root
growth and distribution (Semchenko, John, & Hutchings, 2007; Semchenko,
Saar, & Lepik, 2014), ameliorating the negative effects of root
competition (File, Murphy, & Dudley, 2012). Roots from distantly
related rice plants may grow towards each other while closely related
roots exhibit avoidance, minimizing intraspecific competition (Yang, Li,
Xu, & Kong, 2018). Reduced competition among kin in cultivar mixtures
allowed individuals to better cope with interspecific competition.
Soil microorganisms may contribute
to the coexistence of plant species (Miki, Ushio, Fukui, & Kondoh,
2010). The effects of kin on rice performance and interaction with weeds
may have been partly driven by soil microbial composition. Soil
microbial composition is closely associated with plant species and their
root exudate metabolites (Hu et al., 2018; Schnitzer et al., 2011). In
particular, root exudate metabolites drive plant-soil feedbacks by
shaping the rhizosphere microbiota (Hu et al., 2018), impacting plant
growth and chemical defense traits (Formenti et al., 2021). In the
presence of competing barnyardgrass, allelopathic rice generated
cultivar-specific soil microbial communities that can induce positive
feedbacks on growth and reproduction (Sun, Wang, & Kong, 2014). The
present data show that kin
cultivar mixtures are capable of recruiting and assembling a similar
soil microbial community in which they are able to thrive. Kin effects
mainly occur in the preferred soil where
competitor
relatedness
alters local soil conditions, causing indirect soil effects on
plant
coexistence (Ehlers, David, Damgaard, & Lenormand, 2016). Therefore,
kin cultivar mixtures may create a better soil microbial community for
rice growth.
An additional source of fitness variation in plants growing with
relatives arises from the trade-off in the allocation of plant
carbon and nitrogen (File, Murphy,
& Dudley, 2012). Recent studies have indicated the importance of
nitrogen partitioning and cycling in kin recognition (Semchenko, Saar,
S., & Lepik, 2017; Zhang, Liu, Tian, Xu, & Ouyang, 2016). In this
study, kin cultivar mixtures always had stronger inhibition on
barnyardgrass than non-kin cultivar mixtures, regardless of available
nitrogen.
However, nitrogen application generated carbon and nitrogen allocation
shifts of barnyardgrass from shoots into roots. These results imply that
nitrogen acquisition and partitioning may function independently in
intraspecific kin recognition and interspecific allelopathy.
Allelopathic rice cultivars differentially respond to kin and non-kin by
altering the release of nitrogen-rich allantoin, releasing more
allantoin in the presence of distantly related cultivars (Yang, Li, Xu,
& Kong, 2018). In this study, allantoin application appeared to
alleviate inhibitory differences between kin and non-kin cultivar
mixtures and did not affect the carbon and nitrogen partitioning of
barnyardgrass. Allantoin may act as a transportable nitrogen or signal
to protect plants from stresses (Nourimand & Todd, 2016), activating
the jasmonic acid signaling pathway (Takagi et al., 2016). Rice
cultivars produce and release allantoin in response to species
interactions (Wang, Kong, Hu, & Xu, 2007), inducing changes in
microbial diversity and community composition in soil (Wang, Kong, Sun,
& Xu, 2010). In this study, allantoin was not a transportable source of
nitrogen, but may serve as signaling chemical in response to kin
recognition. However, the role of allantoin as a signal of relatedness
still needs to be verified in cultivar specific or upstream signals.
Allantoin may not be the signal but rather the effect of an
unidentified, underlying signal (Wang, Kong, Wang, & Meiners, 2020).