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\begin{document}

\title{Kin discrimination in allelopathy and consequences for agriculture}



\author[1]{Niels Anten}%
\author[2]{Bin Chen}%
\affil[1]{Wageningen University}%
\affil[2]{Nanjing Forestry University}%


\vspace{-1em}



  
  \date{May 16, 2024}


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\selectlanguage{english}
\begin{abstract}
Recent research has shown that plants can distinguish
genetically-related individuals from strangers (kin recognition) and
exhibit more cooperative behaviours towards these more related
individuals (kin discrimination). The first evidence for this was found
when Cakile edentula plants growing with half-sibs allocated relatively
less biomass to roots than plants growing with unrelated individuals,
indicating that kin recognition can reduce the intensity of competition
(Dudley \& File, 2007). Since then, kin discrimination has been shown to
result in reduced competition for soil resources (Semchenko, Saar, \&
Lepik, 2014), light (Crepy \& Casal, 2015) and pollinators (Torices,
G\selectlanguage{ngerman}ómez, \& Pannell, 2018). On the other hand, allelopathy, plants
producing chemical compounds that negatively affect performance of
neighbour plants, has also been widely documented (Inderjit \& Duke,
2003) and shown to profoundly affect local species coexistence and plant
community structure (Meiners, Kong, Ladwig, Pisula, \& Lang, 2012). In
crops allelopathy can also be beneficial in suppressing weeds (Macías,
Mejías, \& Molinillo, 2019). In the current issue, Xu, Cheng, Kong, and
Meiners (2021) published the first study to show that kin discrimination
can also affect the balance between direct competition for resources and
allelopathy, and this together may lead to improved weed suppression in
rice.%
\end{abstract}\selectlanguage{ngerman}%



\sloppy


\textbf{Kin discrimination in allelopathy and consequences for
agriculture.}

Niels P. R. Anten\textsuperscript{1,*} \& Bin J. W.
Chen\textsuperscript{2}

\textsuperscript{1} Centre for Crop Systems Analysis, Wageningen
University, Wageningen, the Netherlands

\textsuperscript{2} College of Biology and the Environment, Nanjing
Forestry University, Nanjing, China

*Correspondence author: Centre for Crop Systems Analysis, Wageningen
University, Droevendaalsesteeg 1, 6708PB Wageningen, the Netherlands

Recent research has shown that plants can distinguish
genetically-related individuals from strangers (kin recognition) and
exhibit more cooperative behaviours towards these more related
individuals (kin discrimination). The first evidence for this was found
when \emph{Cakile edentula} plants growing with half-sibs allocated
relatively less biomass to roots than plants growing with unrelated
individuals, indicating that kin recognition can reduce the intensity of
competition (Dudley \& File, 2007). Since then, kin discrimination has
been shown to result in reduced competition for soil resources
(Semchenko, Saar, \& Lepik, 2014), light (Crepy \& Casal, 2015) and
pollinators (Torices, G\selectlanguage{ngerman}ómez, \& Pannell, 2018). On the other hand,
allelopathy, plants producing chemical compounds that negatively affect
performance of neighbour plants, has also been widely documented
(Inderjit \& Duke, 2003) and shown to profoundly affect local species
coexistence and plant community structure (Meiners, Kong, Ladwig,
Pisula, \& Lang, 2012). In crops allelopathy can also be beneficial in
suppressing weeds (Macías, Mejías, \& Molinillo, 2019). In the current
issue, Xu, Cheng, Kong, and Meiners (2021) published the first study to
show that kin discrimination can also affect the balance between direct
competition for resources and allelopathy, and this together may lead to
improved weed suppression in rice.

Xu et al. grew target plants of two rice cultivars known to be both
allelopathic and capable of kin recognition, with four different
neighbour-plant treatments in order of decreasing relatedness:
neighbours being of the same cultivar, a genetically closely-related
cultivar, a genetically more distant cultivar but of the same ecotype
(`indica') or of a different type (`japonica'). They explored: root
allocation, allelopathy, weed suppression and biomass production of
target plants in these treatments. They found that plants grown with
neighbouring rice plants of the same cultivar or a closely-related
cultivar allocated their roots less towards neighbouring rice plants but
more towards weeds, with a consequence of greater suppression of the
weeds. This showed that kin interaction could lead to reduced
intraspecific and more effective interspecific competition, consistent
with results from wild plants Semchenko et al. (2014). However, results
for allelopathy were less clear. Rice plants produced less
allelochemicals when growing with neighbours of a closely-related
cultivar than when growing with less related ones, but produced the
highest level when growing with neighbours of the same cultivar. This
indicates that the pattern through which kin recognition may affect
allopathy is still unclear. Moreover, despite of the differences in root
allocation, allelochemical production and weed suppression among
treatments, there was no clear pattern in grain production of rice
plants across treatments. This could imply that weed suppression did not
contribute to yields. It could also be that more related individuals
being phenotypically more similar competed more intensively for e.g.
light, a phenomenon known as kin competition (Platt \& Bever, 2009), so
that positive kin cooperative effects and negative kin competitive
effects compensated each other in their effects on yield (Anten \& Chen,
2021).

\emph{Implications for ecological weed control in agricultural crops}

Farmers generally aim to maximize performance (e.g. yields or
resource-use efficiency) at the crop stand (hence, plant population)
level. This may be in conflict with the fact that in dense vegetation
natural selection favours the most competitive plants rather than those
maximizing group performance (see Anten \& Vermeulen 2016; Denison,
2011). As kin selection can lead to more cooperative traits in plants
and greater group performance, its potential use in crop breeding could
be considered (Anten \& Chen, 2021; Murphy, Van Acker, Rajcan, \&
Swanton, 2017). The results of Xu et al. are particularly interesting in
this regard. Among all biotic stress types (i.e. pathogens, pests and
weeds), weeds have the largest potential for yield reduction (larger
than the other two stress types combined) (Oerke, 2006). Chemical
control of weeds is coming under increasing pressure due to concerns
about their health- and environmental impacts and increasing herbicide
resistance of weeds. This in turn, has led to an increased interest in
ecological weed control, of which development of weed-suppressive crops
can be an important part (Bastiaans, Paolini, \& Baumann, 2008). Thus,
if kin discrimination can reduce intraspecific competition among crop
plants in favour of interspecific competition with weeds as shown by Xu
et al., this could be part of a strategy for ecological weed control.

The question however is whether kin selection is the most effective
means of obtaining cooperative crop types. Conceptually, kin
discriminating plants can be considered as facultative co-operators,
that is, they exhibit cooperative behaviours only in the presence of kin
and not in the presence of non-kin. In a crop variety mixture such a
facultative co-operator may do worse than an obligate co-operator, i.e.,
a crop type that expresses cooperative behaviours irrespective of
whether it interacts with kin or non-kin (Anten \& Chen, 2021). Thus,
the question arises whether preferential root placement towards the
roots of weeds rather than towards con-specific crop plants could also
be selected as a constitutive trait.

\emph{Quantifying benefits of kinship dependent variation in
allelopathy}

Plants produce a wide variety of allelopathic compounds which can have
negative effects on con-specific plants or negative effects on
hetero-specific plants, the former also being called autotoxicity.
Autotoxicity has been documented in a wide variety of plants and is
thought as a mechanism to avoid local intraspecific competition and thus
ensure a greater spatial and temporal seed dispersal (Singh, Batish, \&
Kohli, 1999). It is also well documented in several crops including rice
(Singh et al., 1999) and is believed as an important cause of yield
reductions in continuous mono-cropping (i.e., growing the same crop on a
field year after year, Chi et al., 2013). Xu et al.'s finding of reduced
allelopathic activities in rice plants only interacting with
closely-related-cultivar neighbours may suggest this reduction to
reflect a kinship-selected cooperative strategy avoiding auto-toxic
effects on kin. However, this raises the question why the highest
allelopathic activities were found in plants interacting with neighbours
of the same cultivar (i.e., the treatment with the greatest degree of
neighbour relatedness).Recent research has shown for wheat that plants
may produce allelochemicals in response to exudates produced by
neighbours, particularly loliolide and jasmonic acid (Kong et al.,
2018). It is possible that such signalling also occurs in rice and that
it differs between cultivars, independently of relatedness, and that the
two focal cultivars in Xu et al. (2021) may have happened to be active
producers of such signalling compounds. Clearly, more research is needed
to better understand the possible connection between kin recognition and
allopathy.

\emph{Towards a quantitative approach to research on kin recognition}

Since the first documentation if kin recognition in plants (Dudley \&
File, 2007), and despite of mounting interest on this topic, there is
still no consensus on how to define the distinction between `kin' and
`non-kin'. Many studies, especially those on wild species, reserve the
word `kin' for plants sharing the same mother, being either sibs or
half-sibs (e.g. Lepik, Abakumova, Zobel, \& Semchenko, 2012; Semchenko
et al., 2014; Torices et al., 2018). But several studies with crop
species also categorise kin and non-kin at the cultivar or variety level
(e.g. Pezzola, Pandolfi, \& Mancuso, 2020), while studies using the
model species \emph{Arabidopsis thaliana} separate kin and non-kin at
the accession level (e.g, Biedrzycki, Jilany, Dudley, \& Bais, 2010;
Palmer et al., 2016). This variation in definition makes it difficult to
compare results across studies, and could explain some of the
discrepancies between different studies. Moreover, most studies on kin
discrimination simply compare trait values and performance between
discrete kin- and non-kin groups, often without actually quantifying the
level of genetic relatedness (but see Karban, Shiojiri, Ishizaki,
Wetzel, \& Evans, 2013 and Xu et al., 2021 as notable exception). As
kinship describes the extent of genetic similarity between individuals,
it is rather arbitrary to categorise this relationship. We therefore
propose that kinship should be expressed as a continuous quantitative
measure in terms of genetic relatedness.

Furthermore, the level of replication at the genotypic is often
insufficient (rarely more than 10 genotypes) to determine robust
correlations of trait expression at different levels of relatedness. To
our opinion addressing questions about kin discrimination and its
consequences for agricultural or fitness entails firstly quantifying
genetic variation in kin discrimination within a sufficiently large
population of plants, and secondly, determining whether this variation
correlates positively with performance in kin groups. We thus urge for a
broader quantitative genetic approach to the research on the selection
effects of kin recognition.

\textbf{Keywords} : allelopathy, Darwinian agriculture, ecological weed
control, interference competition, kin recognition, rice

\textbf{Acknowledgements}

We thank the National Natural Science Foundation of China (32071526) for
support. There is no conflict of interest.

\textbf{Data availability}

The paper did not use data.

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