Identification of ABA-mediated genetic and metabolic responses to soil flooding in tomato (Solanum lycopersicum L. Mill)

Soil flooding is a compound abiotic stress that alters soil properties and limits atmospheric gas diffusion (O2 and CO2) to the roots. The involvement of abscisic acid (ABA) in the regulation of soil flooding-specific genetic and metabolic responses has been scarcely studied despite its key importance as regulator in other abiotic stress conditions. To attain this objective, wild type and ABA-deficient tomatoes were subjected to short-term (24 h) soil waterlogging. After this period, gas exchange parameters were reduced in the wild type but not in ABA-deficient plants that always had higher E and gs. Transcript and metabolite alterations were more intense in waterlogged tissues, with genotype-specific variations. Waterlogging reduced the ABA levels in the roots while inducing PYR/PYL/RCAR ABA receptors and ABA-dependent transcription factor transcripts, of which induction was less pronounced in the ABA-deficient genotype. Ethylene/O2-dependent genetic responses (ERFVIIs, plant anoxia survival responses, and genes involved in the N-degron pathway) were induced in hypoxic tissues independently of the genotype. Interestingly, genes encoding a nitrate reductase and a phytoglobin involved in NO biosynthesis and scavenging and ERFVII stability were induced in waterlogged tissues, but to a lower extent in ABA-deficient tomato. At the metabolic level, flooding-induced accumulation of Ala was enhanced in ABA-deficient lines following a differential accumulation of Glu and Asp in both hypoxic and aerated tissues, supporting their involvement as sources of oxalacetate to feed the tricarboxylic acid cycle in waterlogged tissues and constituting a potential advantage upon long periods of soil waterlogging. The promoter analysis of upregulated genes indicated that the production of oxalacetate from Asp via Asp oxidase, energy processes such as acetyl-CoA, ATP, and starch biosynthesis, and the lignification process were likely subjected to ABA regulation. Taken together, these data indicate that ABA depletion in waterlogged tissues acts as a positive signal, inducing several specific genetic and metabolic responses to soil flooding.

This work was supported by the Spanish Ministerio de Economía y Competitividad, Universitat Jaume I and Generalitat Valenciana/Fondo Europeo de Desarrollo Regional (FEDER), co-funded through grant nos. AGL2016-76574-R, UJI-B2016-23, UJI-B2016-24, IDIFEDER/2018/010, and UJI-B2019-24 to AG-C, VA, and MG-G, respectively. CD was supported by UJI PICD program. MG-G and JM were supported by Ramon y Cajal contracts from Spanish Ministerio de Economía y Competitividad (RYC-2016-19325 and RYC-2017-23645, respectively). JR was supported by a Juan de la Cierva-Formación contract from the Spanish Ministerio de Economía y Competitividad (FJCI-2016-28601).

Peer reviewed