Introduction
Plasticity is the ability of an organism to produce diverse phenotypes
in response to changes in the environment. For sessile organisms such as
plants, plasticity is particularly advantageous as it allows rapid
adjustment to different environments. Nitrogen (N) is an essential
component for the production of amino acids, nucleic acids, and
chlorophyll, and thus directly affects plant growth and development
(Guignard et al., 2017; Oldroyd & Leyser, 2020). Plants take up N from
the soil primarily as ammonium and nitrate. N distribution in soil
varies both in time and in space resulting in uneven growth among
individuals, populations and species (Lark et al., 2004; Pandey et al.,
2019). In agriculture, stable crop growth and yield are ensured by
applying fertilizers that contain N. However, losses of the large amount
of N supplied via fertilization to the environment negatively impact
entire ecosystems (Guignard et al., 2017; McAllister, Beatty, & Good,
2012). One route towards improved yield without addition of fertilizers
is to understand the mechanisms underlying plant plasticity responses to
N availability. This will allow the development of crop lines with
stable growth under varying and unpredictable N availability.
The gene regulatory and metabolic networks for N uptake, assimilation
and utilization are well characterized and have been used to improve
nitrogen use efficiency (NUE) in plants (Arsova, Kierszniowska, &
Schulze, 2012; Fredes, Moreno, Diaz, & Gutierrez, 2019; Gutierrez,
2012; Krapp et al., 2011; Li, Hu, & Chu, 2017; Meyer et al., 2019;
Vidal & Gutierrez, 2008). For instance, modifying the transport of
amino acids has been employed to improve NUE in pea (Perchlik &
Tegeder, 2017). Similarly, DNA methylation and epigenetic mechanisms
were found to contribute to the modulation of NUE (Kuhlmann et al.,
2020). Given the tight coordination between carbon and N metabolism,
genetically improving photosynthesis may also increase NUE and reduce
the necessity of fertilizers (Evans & Clarke, 2018). It was also
demonstrated that the plasticity in growth-related traits in response to
N availability varies between local populations of Arabidopsis
thaliana (Arabidopsis) (Pandey et al., 2019). Further, Arabidopsis
accessions cope with differences in N availability by modifying the root
and shoot architecture, growth, and biomass (de Jong et al., 2019;
Ikram, Bedu, Daniel-Vedele, Chaillou, & Chardon, 2012;
Masclaux-Daubresse & Chardon, 2011; Meyer et al., 2019; North, Ehlting,
Koprivova, Rennenberg, & Kopriva, 2009). However, the question of
whether or not there are genes that control plasticity of different
focal traits to N availability remains open. The availability of
accessions, as genetically homozygous lines (Kramer, 2015; Weigel,
2012), along with a large repertoire of genetic and molecular tools,
renders Arabidopsis an excellent model system to address this question.
Despite the high potential of genome-wide association (GWA) in
identifying genetic basis of phenotypic variation, only a few studies
have used this approach to investigate genotype variation in plasticity
among Arabidopsis accessions (Brachi, Faure, Bergelson, Cuguen, & Roux,
2013; de Jong et al., 2019; Sasaki, Zhang, Atwell, Meng, & Nordborg,
2015). A challenge for mapping genes that control plasticity, hereafter
referred to as plasticity genes, lies in the quantification of
plasticity as a trait. Plasticity can be quantified by different
approaches, including, but not limited to linear regression of the
reaction norms, the coefficient of variation (CV), plasticity index, and
fold change (FC) (Laitinen & Nikoloski, 2019; Pennacchi et al., 2020).
Here we focus on dissecting the genetic architecture of plasticity of
growth- and flowering- related traits in response to the availability of
N in the soil in a panel of Arabidopsis accessions. Since growth and
development are tightly linked to metabolism, we also asked if the
plasticity of growth- and flowering-related traits could be explained by
the plasticity of primary metabolites. Finally, we investigated if the
studied plasticities were specific for different environmental cues,
including light and day length. Our GWA study revealed that the genetic
architecture of the studied plasticities differed. We identified thatAt1g19880 , gene encoding for a RCC1 family protein, is involved
in controlling the plasticity of rosette size in the beginning of the
vegetative growth in response to N. Additionally, our results indicated
that the mechanisms controlling the plasticity of plant size and
flowering time to N availability are independent from other
growth-limiting environmental cues, such as light.