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.