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Review
. 2023 Nov 13;4(6):100571.
doi: 10.1016/j.xplc.2023.100571. Epub 2023 Mar 7.

Chasing the mechanisms of ecologically adaptive salinity tolerance

Affiliations
Review

Chasing the mechanisms of ecologically adaptive salinity tolerance

Silvia Busoms et al. Plant Commun. .

Abstract

Plants adapted to challenging environments offer fascinating models of evolutionary change. Importantly, they also give information to meet our pressing need to develop resilient, low-input crops. With mounting environmental fluctuation-including temperature, rainfall, and soil salinity and degradation-this is more urgent than ever. Happily, solutions are hiding in plain sight: the adaptive mechanisms from natural adapted populations, once understood, can then be leveraged. Much recent insight has come from the study of salinity, a widespread factor limiting productivity, with estimates of 20% of all cultivated lands affected. This is an expanding problem, given increasing climate volatility, rising sea levels, and poor irrigation practices. We therefore highlight recent benchmark studies of ecologically adaptive salt tolerance in plants, assessing macro- and microevolutionary mechanisms, and the recently recognized role of ploidy and the microbiome on salinity adaptation. We synthesize insight specifically on naturally evolved adaptive salt-tolerance mechanisms, as these works move substantially beyond traditional mutant or knockout studies, to show how evolution can nimbly "tweak" plant physiology to optimize function. We then point to future directions to advance this field that intersect evolutionary biology, abiotic-stress tolerance, breeding, and molecular plant physiology.

Keywords: adaptation; ecology; evolution; microbiome; polyploidy; salinity.

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Figures

Figure 1
Figure 1
Schematic of mechanisms of adaptive salt tolerance. Consider the pictured landscape. Seawater provides a source of sodium ions; wind carries sea spray inland, creating a gradient of soil salinity. Ancestral populations of wild plant species originated inland. In this population, we observe standing variation, which is affected by de novo mutation and purifying selection, removing any alleles that come with a fitness disadvantage, or, in other words, that are maladaptive (e.g., AtHKT1HLS). Plant populations then by chance migrate to the seaside, possibly due to seeds being carried by humans or other animals. This derived population will represent a subset of the standing variation observed in the ancestral population. If it carries some of the rarer alleles, which are under purifying selection further inland, due to the high cost associated with them, these alleles could now be under positive selection if they are adaptive in the new location. These alleles would become fixed in this new habitat (e.g., GsERD15BIns). Under this scenario the effective population size decreases, the phenotype becomes much more constant, and plasticity is reduced. Other realistic scenarios include migrants harboring these alleles at a much higher frequency representing stepping stones in that direction. In these migrants, balancing selection maintains a relatively high frequency of an allele. This could reflect the allele being required at certain times in the year or in certain challenging but regular events (e.g., mixed population of AtHKT1HLSand AtHKT1LLS).
Figure 2
Figure 2
Experimental setup for a microbiome reciprocal transplant. Salt-adapted and salt-sensitive plants cultivated in sterile saline or sterile non-saline soil will be non-inoculated (N/I), inoculated with their own microbiome (saline microbiome [S–M] or non-saline microbiome [NS-M]), or inoculated with the opposite microbiome, in each of the four scenarios.

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