The plant root is the first organ to encounter salinity stress, but the effect of salinity on root system architecture (
RSA) remains elusive. Both the reduction in main root (
MR) elongation and the redistribution of the root mass between
MRs and lateral roots (
LRs) are likely to play crucial roles in water extraction efficiency and ion exclusion. To establish which
RSA parameters are responsive to salt stress, we performed a detailed time course experiment in which Arabidopsis (
Arabidopsis thaliana) seedlings were grown on agar plates under different salt stress conditions. We captured
RSA dynamics with quadratic growth functions (
root-fit) and summarized the salt-induced differences in
RSA dynamics in three growth parameters:
MR elongation, average
LR elongation, and increase in number of
LRs. In the ecotype Columbia-0 accession of Arabidopsis, salt stress affected
MR elongation more severely than
LR elongation and an increase in
LRs, leading to a significantly altered
RSA. By quantifying
RSA dynamics of 31 different Arabidopsis accessions in control and mild salt stress conditions, different strategies for regulation of
MR and
LR meristems and root branching were revealed. Different
RSA strategies partially correlated with natural variation in abscisic acid sensitivity and different Na
+/K
+ ratios in shoots of seedlings grown under mild salt stress. Applying
root-fit to describe the dynamics of
RSA allowed us to uncover the natural diversity in root morphology and cluster it into four response types that otherwise would have been overlooked.Salt stress is known to affect plant growth and productivity as a result of its osmotic and ionic stress components. Osmotic stress imposed by salinity is thought to act in the early stages of the response, by reducing cell expansion in growing tissues and causing stomatal closure to minimize water loss. The build-up of ions in photosynthetic tissues leads to toxicity in the later stages of salinity stress and can be reduced by limiting sodium transport into the shoot tissue and compartmentalization of sodium ions into the root stele and vacuoles (
Munns and Tester, 2008). The effect of salt stress on plant development was studied in terms of ion accumulation, plant survival, and signaling (
Munns et al., 2012;
Hasegawa, 2013;
Pierik and Testerink, 2014). Most studies focus on traits in the aboveground tissues, because minimizing salt accumulation in leaf tissue is crucial for plant survival and its productivity. This approach has led to the discovery of many genes underlying salinity tolerance (
Munns and Tester, 2008;
Munns et al., 2012;
Hasegawa, 2013;
Maathuis, 2014). Another way to estimate salinity stress tolerance is by studying the rate of main root (
MR) elongation of seedlings transferred to medium supplemented with high salt concentration. This is how Salt Overly Sensitive mutants were identified, being a classical example of genes involved in salt stress signaling and tolerance (
Hasegawa, 2013;
Maathuis, 2014). The success of this approach is to be explained by the important role that the root plays in salinity tolerance. Roots not only provide anchorage and ensure water and nutrient uptake, but also act as a sensory system, integrating changes in nutrient availability, water content, and salinity to adjust root morphology to exploit available resources to the maximum capacity (
Galvan-Ampudia et al., 2013;
Gruber et al., 2013). Understanding the significance of environmental modifications of root system architecture (
RSA) for plant productivity is one of the major challenges of modern agriculture (
de Dorlodot et al., 2007;
Den Herder et al., 2010; Pierik and Testerink, 2014).The
RSA of dicotyledonous plants consists of an embryonically derived
MR and lateral roots (
LRs) that originate from xylem pole pericycle cells of the
MR, or from
LRs in the case of higher-order
LRs. Root growth and branching is mainly guided through the antagonistic action of two plant hormones: auxin and cytokinins (
Petricka et al., 2012). Under environmental stress conditions, the synthesis of abscisic acid (
ABA), ethylene, and brassinosteroids is known to be induced and to modulate the growth of
MRs and
LRs (
Achard et al., 2006;
Osmont et al., 2007;
Achard and Genschik, 2009;
Duan et al., 2013;
Geng et al., 2013). In general, lower concentrations of salt were observed to slightly induce
MR and
LR elongation, whereas higher concentrations resulted in decreased growth of both
MRs and
LRs (
Wang et al., 2009;
Zolla et al., 2010). The reduction of growth is a result of the inhibition of cell cycle progression and a reduction in root apical meristem size (
West et al., 2004). However, conflicting results were presented for the effect of salinity on lateral root density (
LRD;
Wang et al., 2009;
Zolla et al., 2010;
Galvan-Ampudia and Testerink, 2011). Some studies suggest that mild salinity enhances
LR initiation or emergence events, thereby affecting patterning, whereas other studies imply that salinity arrests
LR development. The origin of those contradictory observations could be attributable to studying
LR initiation and density at single time points, rather than observing the dynamics of
LR development, because
LR formation changes as a function of root growth rate (
De Smet et al., 2012). The dynamics of
LR growth and development were characterized previously for the
MR region formed before the salt stress exposure, identifying the importance of
ABA in early growth arrest of postemerged
LRs in response to salt stress (
Duan et al., 2013). The effect of salt on
LR emergence and initiation was found to differ for
MR regions formed prior and subsequent to salinity exposure (
Duan et al., 2013), consistent with
LR patterning being determined at the root tip (
Moreno-Risueno et al., 2010). Yet the effect of salt stress on the reprogramming of the entire
RSA on a longer timescale remains elusive.Natural variation in Arabidopsis (
Arabidopsis thaliana) is a great source for dissecting the genetic components underlying phenotypic diversity (
Trontin et al., 2011;
Weigel, 2012). Genes underlying phenotypic plasticity of
RSA to environmental stimuli were also found to have high allelic variation leading to differences in root development between different Arabidopsis accessions (
Rosas et al., 2013). Supposedly, genes responsible for phenotypic plasticity of the root morphology to different environmental conditions are under strong selection for adaptation to local environments. Various populations of Arabidopsis accessions were used to study natural variation in ion accumulation and salinity tolerance (
Rus et al., 2006;
Jha et al., 2010;
Katori et al., 2010;
Roy et al., 2013). In addition, a number of studies focusing on the natural variation in
RSA have been published, identifying quantitative trait loci and allelic variation for genes involved in
RSA development under control conditions (
Mouchel et al., 2004;
Meijón et al., 2014) and nutrient-deficient conditions (
Chevalier et al., 2003;
Gujas et al., 2012;
Gifford et al., 2013;
Kellermeier et al., 2013;
Rosas et al., 2013). Exploring natural variation not only expands the knowledge of genes and molecular mechanisms underlying biological processes, but also provides insight on how plants adapt to challenging environmental conditions (
Weigel, 2012) and whether the mechanisms are evolutionarily conserved. The early growth arrest of newly emerged
LRs upon exposure to salt stress was observed to be conserved among the most commonly used Arabidopsis accessions Columbia-0 (
Col-0), Landsberg
erecta, and Wassilewskija (Ws;
Duan et al., 2013). By studying salt stress responses of the entire
RSA and a wider natural variation in root responses to stress, one could identify new morphological traits that are under environmental selection and possibly contribute to stress tolerance.In this work, we not only identify the
RSA components that are responsive to salt stress, but we also describe the natural variation in dynamics of salt-induced changes leading to redistribution of root mass and different root morphology. The growth dynamics of
MRs and
LRs under different salt stress conditions were described by fitting a set of quadratic growth functions (
root-fit) to individual
RSA components. Studying salt-induced changes in
RSA dynamics of 31 Arabidopsis accessions revealed four major strategies conserved among the accessions. Those four strategies were due to differences in salt stress sensitivity of individual
RSA components (i.e. growth rates of
MRs and
LRs, and increases in the number of emerged
LRs). This diversity in root morphology responses caused by salt stress was observed to be partially associated with differences in
ABA, but not ethylene sensitivity. In addition, we observed that a number of accessions exhibiting a relatively strong inhibition of
LR elongation showed a smaller increase in the Na
+/K
+ ratio in shoot tissue after exposure to salt stress. Our results imply that different
RSA strategies identified in this study reflect diverse adaptations to different soil conditions and thus might contribute to efficient water extraction and ion compartmentalization in their native environments.
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