Keeping the shoot above water – submergence triggers antithetical growth responses in stems and petioles of watercress (Nasturtium officinale)

Abstract

The molecular mechanisms controlling underwater elongation are based extensively on studies on internode elongation in the monocot rice (Oryza sativa) and petiole elongation in Rumex rosette species. Here, we characterize underwater growth in the dicot Nasturtium officinale (watercress), a wild species of the Brassicaceae family, in which submergence enhances stem elongation and suppresses petiole growth. We used a genome-wide transcriptome analysis to identify the molecular mechanisms underlying the observed antithetical growth responses. Though submergence caused a substantial reconfiguration of the petiole and stem transcriptome, only little qualitative differences were observed between both tissues. A core submergence response included hormonal regulation and metabolic readjustment for energy conservation, whereas tissue-specific responses were associated with defense, photosynthesis, and cell wall polysaccharides. Transcriptomic and physiological characterization suggested that the established ethylene, abscisic acid (ABA), and GA growth regulatory module for underwater elongation could not fully explain underwater growth in watercress. Petiole growth suppression is likely attributed to a cell cycle arrest. Underwater stem elongation is driven by an early decline in ABA and is not primarily mediated by ethylene or GA. An enhanced stem elongation observed in the night period was not linked to hypoxia and suggests an involvement of circadian regulation.

Two Brassica napus cultivars differ in gene expression, but not in their response to submergence

“…The low availability of sugars as well as the down‐regulation of biosynthetic processes and translation prompted us to test how much the growth of Brassica napus was affected under submergence. For other plant species like Rumex palustris , rice or the Brassicaceae N. officinale , enhanced elongation of stems or petioles has been described (summarized in Voesenek & Bailey‐Serres, 2015; Mustroph, 2018; Müller et al, 2019). Therefore, we determined the growth of the hypocotyl and the petioles of submerged B. napus plants within a two‐week treatment.…”

“…Other HRGs like ADH ( AT1G77120 ) or the LOB DOMAIN‐CONTAINING PROTEIN 41 ( AT3G02550 ) are not induced in our submergence treatment, or under carbon starvation (Figures S4, S11). Those genes are significantly induced by submergence in darkness (van Veen et al, 2016, Figure S11), but not by submergence in light (Figure S4, Müller et al, 2019). In addition to gene expression, we analyzed the activity of the fermentation enzyme ADH, which was not modified under submergence (Figure 5).…”

“…The selection of differentially expressed genes, gene ontology (GO) term enrichments as well as gene annotations was performed as described in detail in a study on N. officinale (Müller et al, 2019). Data have been deposited at the Gene Expression Omnibus database under the accession GSE140828.…”

“…Under these circumstances, avoidance mechanisms of the shoots are required, that is, elongation growth of stems and/ or petioles or the formation of leaf gas films. Recently, we identified the molecular response of the flood‐tolerant Brassicaceae N. officinale and identified it as a species with a submergence escape response (Müller et al, 2019). The response of the related Brassicaceae B. napus to submergence has not been investigated yet.…”

Plant performance and food security in a wetter world

“…However, as Müller et al . (2021, in this issue) discovered, in some species such as Nasturtium officinale (watercress), the growth control machinery is wired differently. Interestingly in watercress, submergence triggered opposing growth responses in the stems and petioles.…”