Divergence in a stress regulatory network underlies differential growth control

Abstract

The use of marginal lands in agriculture is increasingly necessary to support the global human population. Elevated salinity frequently occurs in degraded soils and hinders their use due to the negative impact salt stress has on plant growth. While the hormonal networks controlling growth have been extensively characterized in stress-sensitive plants, it is unclear how these pathways are rewired in plants that maintain growth in extreme environments. We have compared the physiological and molecular responses of four closely related members of the Brassicaceae family including two salt-tolerant species (Shrenkiella parvula and Eutrema salsugineum) and two salt-sensitive species (Sisymbrium irio and Arabidopsis thaliana) to the salt stress-induced hormone, abscisic acid (ABA). While ABA inhibits root growth in most species, we uncovered substantial growth-promoting effects in Shrenkiella parvula, due to an enhancement in cell elongation. Comparative transcriptomics informed by phylogenetic relationships uncovered lineage and extremophile-specific differences in ABA response. DNA Affinity Purification followed by sequencing (DAP-Seq) was utilized to establish gene regulatory networks (GRNs) in each species for the entire ABA-RESPONSIVE ELEMENT BINDING FACTORS (AREB/ABF) clade. Comparative GRN analysis identified relative conservation in the core ABA signaling GRN, while the auxin growth-hormone GRN was highly divergent, revealing how patterns of gain and loss of cis-regulatory elements mediate novel physiological outcomes. Our findings demonstrate that the targets of hormone signaling pathways are highly divergent between species and that diametric inversion of growth regulation is possible, even between closely related species of the same plant family.

Multiple paths lead to salt tolerance - pre-adaptation vs dynamic responses from two closely related extremophytes

“…Compared to A. thaliana , KAT1 is highly expressed at basal expression in the roots of both extremophytes (Figure 6A). Notably, the expression of these K channels is regulated by ABA and auxin signaling pathways, which are modified in both extremophytes compared to A. thaliana in conjunction with root growth modulation in response to salt (Figures 4, S7, and 7) 47 . Intracellular K transport, as seen with KEA5 (a K transporter in the trans-Golgi network) and KUP9 (mediates K and auxin transport from the endoplasmic reticulum) 34, 48 appear to be differently regulated between the extremophytes and A. thaliana (Figures 6A and 7).…”

Burning questions for a warming and changing world: 15 unknowns in plant abiotic stress

“…The sequencing of over 1,000 accessions facilitated the identification of genetic loci under selection, and identified the ABA signaling pathway as being important (1001Genomes Consortium, 2016. ABA, which is induced under drought and salinity stress (Cutler et al, 2010), suppresses root growth in Arabidopsis, particularly at concentrations above 1 mM, while in other species like S. parvula, an extremophyte plant living at the edge of a hyper-saline lake, ABA accelerates growth (Sun et al, 2022). These data suggest that even for well-characterized signaling pathways, diametric changes in response to ABA are possible.…”

“…This provides insight into the diversification of cell type functions and the potential discovery of new cell types. DNA affinity purification and sequencing (DAP-seq), which allows for the in vitro reconstitution of transcription factor-genome interactions (O'Malley et al, 2016), enables the determination of GRNs in nonmodel species (Sun et al, 2022). Comparisons of GRN architecture between related species provide a means of understanding how the evolution of genomic sequence leads to the rewiring of GRNs and the regulation of downstream physiological processes important for stress acclimation.…”