Hypoxia and the group VII ethylene response transcription factor HRE2 promote adventitious root elongation inArabidopsis

Abstract

Soil water-logging and flooding are common environmental stress conditions that can impair plant fitness. Roots are the first organs to be confronted with reduced oxygen tension as a result of flooding. While anatomical and morphological adaptations of roots are extensively studied, the root system architecture is only now becoming a focus of flooding research. Adventitious root (AR) formation shifts the root system higher up the plant, thereby facilitating supply with oxygen, and thus improving root and plant survival. We used Arabidopsis knockout mutants and overexpressors of ERFVII transcription factors to study their role in AR formation under hypoxic conditions and in response to ethylene. Results show that ethylene inhibits AR formation. Hypoxia mainly promotes AR elongation rather than formation mediated by ERFVII transcription factors, as indicated by reduced AR elongation in erfVII seedlings. Overexpression of HRE2 induces AR elongation to the same degree as hypoxia, while ethylene overrides HRE2-induced AR elongation. The ERFVII transcription factors promote establishment of an AR system that is under negative control by ethylene. Inhibition of growth of the main root system and promotion of AR elongation under hypoxia strengthens the root system in upper soil layers where oxygen shortage may last for shorter time periods.

Tolerant mechanisms to O2 deficiency under submergence conditions in plants

“…Adventitious roots Adventitious roots (ARs) are also associated with conferring developmental plasticity to plants under waterlogged condition. ARs with high porosities emerge from submerged stem nodes and hypocotyls to replace the existing and deteriorating primary root system in rice, R. palustris, Solanum lycopersicum, and Larix laricina (Calvo-Polanco et al 2012;Dawood et al 2014;Dawood et al 2016;Eysholdt-Derzsó and Sauter 2019;Visser et al 1996;Yang et al 2018;Zhang et al 2017) (Fig. 4).…”

“…4). Some ARs develop chloroplasts and thus provide an additional source of O 2 and carbohydrates (Rich et al 2012) because ARs typically develop in well-aerated topsoil layers (Dawood et al 2014;Eysholdt-Derzsó and Sauter 2019;Zhang et al 2015). The terrestrial plant Solanum dulcamara can survive under flooding condition by replacing the original flood-sensitive root system with aerenchymatous ARs that are produced from pre-formed primordia on the stem.…”

“…In Arabidopsis, low levels of ethylene and hypoxia signals mainly promote AR elongation due to the expression of the hypoxia-responsive HRE2 which is one of the ERFVII TFs (Bailey-Serres et al 2012;Eysholdt-Derzsó and Sauter 2019;Hess et al 2011) (Fig. 4).…”

“…Their strategy is called low O 2 escape strategies (LOES). Plants with the LOES phenotypes can change their shoots and roots in response to O 2 deficiency such as shoot elongation, formation of aerenchyma, barriers to radial O 2 loss (ROL) from the roots, formation of adventitious roots (ARs), and maintenance of gas films on leaf surface (Colmer 2003;Eysholdt-Derzsó and Sauter 2019;Sorrell and Hawes 2009;Winkel et al 2013;Winkel et al 2014). Some wetland plants show another strategy, low O 2 quiescence strategy (LOQS).…”

Phytohormone-Mediated Stomatal Response, Escape and Quiescence Strategies in Plants under Flooding Stress

“…Plants try to adapt to these adverse conditions by applying several strategies, like the storage of energy, elongation of the petiole or internodes, maintenance of water level by regulating stomatal movements, the formation of adventitious roots, development of aerenchyma etc. [2][3][4][5]. Crop plants simultaneously activate various biochemical reactions, molecular and signaling pathways, and physiological processes to cope with this oxygen-limiting condition [1,6].…”