Submergence and Waterlogging Stress in Plants: A Review Highlighting Research Opportunities and Understudied Aspects

Abstract

Soil flooding creates composite and complex stress in plants known as either submergence or waterlogging stress depending on the depth of the water table. In nature, these stresses are important factors dictating the species composition of the ecosystem. On agricultural land, they cause economic damage associated with long-term social consequences. The understanding of the plant molecular responses to these two stresses has benefited from research studying individual components of the stress, in particular low-oxygen stress. To a lesser extent, other associated stresses and plant responses have been incorporated into the molecular framework, such as ion and ROS signaling, pathogen susceptibility, and organ-specific expression and development. In this review, we aim to highlight known or suspected components of submergence/waterlogging stress that have not yet been thoroughly studied at the molecular level in this context, such as miRNA and retrotransposon expression, the influence of light/dark cycles, protein isoforms, root architecture, sugar sensing and signaling, post-stress molecular events, heavy-metal and salinity stress, and mRNA dynamics (splicing, sequestering, and ribosome loading). Finally, we explore biotechnological strategies that have applied this molecular knowledge to develop cultivars resistant to flooding or to offer alternative uses of flooding-prone soils, like bioethanol and biomass production.

Keywords: anoxia; biotechnology; cell signaling; hypoxia; stress perception; submergence; waterlogging.

FIGURE 1

Interconnection of different signaling and transduction events during waterlogging/submergence stress. (A) Integration of metabolic pathways (glycolysis, fermentation, nitrogen conservation and assimilation), hormone homeostasis (NO cycle), calcium-mediated energy signaling (Ca²⁺ signaling), transcription factor (TF) abundance (N-terminal rule, NTR) and availability (membrane exclusion), and transcriptional control. (B) Known nuclear interactions of hypoxia/anoxia TFs with regulating proteins. (C) Comparison of the domain structure of RAP2.12, a high-complexity ERF-VII TF (the other being RAP2.2) and RAP2.3, a low-complexity ERF-VII TF (others being HRE1 and HRE2), and details of demonstrated domain functions. 2-OG, 2-oxoglutarate; ACBP, acyl-CoA binding protein; ALAT, alanine aminotransferase; ARC, amidoxime reducing component; CHGs, hypoxia core genes; ERF, ethylene response factor; FAE, fatty acid elongase; GAI, gibberellic acid insensitive; GDH, glutamate dehydrogenase; HB, hemoglobin; HCR1, hydraulic conductivity of the root; HRE1, hypoxia response attenuator; Int., interactor protein; MPK3, MAP kinase 3; NiR, nitrite reductase; NO, nitric oxide; NTR, N-terminal route; PCO, plant cell oxidase; SAB, Sub1A binding.

FIGURE 2

miRNA modulation of known responses to flooding. The name of a miRNA when green or red indicates up- or down-regulation under flooding stress, respectively. The thickness of the arrows indicates the enhancement of the activation/repression activity. Ovals indicate transcription factors while circles indicate enzymes; thick-lined circles indicate targets confirmed in the plant studied. When known, the short-term and long-term expression under flooding stress is indicated. Asterisk indicates a predicted unconfirmed target. AAO, ascorbic acid oxidase; ATPs, ATP sulfurylase; CBP, copper binding protein; GBSS, granule-bound starch synthase; GH, glycosyl hydrolase; LAC, laccase; LRR, leucine-rich repeat; ME, malic enzyme; PLCL, plantacyanin-like protein; POD, peroxidase; SOD, superoxide dismutase; UKN, unknown function protein; β-amy, beta-amylase.