Aerenchymatous phellem in hypocotyl and roots enables O₂ transport in Melilotus siculus

Abstract

Summary• Aerenchymatous phellem (secondary aerenchyma) has rarely been studied in roots. Its formation and role in internal aeration were evaluated for Melilotus siculus, an annual legume of wet saline land.• Plants were grown for 21 d in aerated or stagnant (deoxygenated) agar solutions. Root porosity and maximum diameters were measured after 0, 7, 14 and 21 d of treatment. Phellem anatomy was studied and oxygen (O 2 ) transport properties examined using methylene blue dye and root-sleeving O 2 electrodes.• Interconnecting aerenchymatous phellem developed in hypocotyl, tap root and older laterals (but not in aerial shoots), with radial intercellular connections to steles. Porosity of main roots containing phellem was c. 25%; cross-sectional areas of this phellem were threefold greater for stagnant than for aerated treatments. Root radial O 2 loss was significantly reduced by complete hypocotyl submergence; values approached zero after disruption of hypocotyl phellem below the waterline or, after shoot excision, by covering hypocotyl phellem in nontoxic cream.• Aerenchymatous phellem enables hypocotyl-to-root O 2 transport in M. siculus. Phellem increases radially under stagnant conditions, and will contribute to waterlogging tolerance by enhancing root aeration. It seems likely that with hypocotyl submerged, O 2 will diffuse via surface gas-films and internally from the shoot system.

Waterlogging tolerance in barley is associated with faster aerenchyma formation in adventitious roots

“…Waterlogging-tolerant species, such as the wild relative of barley H. marinum (Garthwaite et al 2003) have significantly higher root porosity than the susceptible species under waterlogging conditions. The linkage between root porosity and waterlogging tolerance were also found in wheat (Mcdonald et al 2001), maize (Mano and Omori 2013), soybean (Shimamura et al 2010) and forage legumes (Gibberd et al 1999;Teakle et al 2011). In our experiments, waterlogging-tolerant barley genotypes had significantly higher root porosity than susceptible genotypes under waterlogging treatment.…”

“…The tolerant genotypes also had a faster increase of root porosity with accelerated aerenchyma development under waterlogging treatment. In legumes, the faster aerenchyma formation is associated with the recovery of N metabolism in roots (Thomas et al 2005) and improves the internal oxygen transport from shoot to waterlogged roots, enhancing an increased concentration of oxygen in the root zone (Shimamura et al 2010;Teakle et al 2011). The waterlogging-tolerant legume Melilotus siculus (Teakle et al 2011) and waterlogging-tolerant soybean genotypes (Shimamura et al 2010;Thomas et al 2005) were able to form aerenchyma rapidly, reaching more than 20 % of porosity after 7 days waterlogging treatment.…”

“…In legumes, the faster aerenchyma formation is associated with the recovery of N metabolism in roots (Thomas et al 2005) and improves the internal oxygen transport from shoot to waterlogged roots, enhancing an increased concentration of oxygen in the root zone (Shimamura et al 2010;Teakle et al 2011). The waterlogging-tolerant legume Melilotus siculus (Teakle et al 2011) and waterlogging-tolerant soybean genotypes (Shimamura et al 2010;Thomas et al 2005) were able to form aerenchyma rapidly, reaching more than 20 % of porosity after 7 days waterlogging treatment. In contrast, less than 10 % of root porosity was detected in the relatively less waterlogging-tolerant wheat (Yamauchi et al 2014) and canola (Voesenek et al 1999) after 7 days of waterlogging treatment.…”

Plants and flooding stress

“…The lack of secondary aerenchyma formation is a major reason for flood intolerance among ‘woody dicots’ (Justin & Armstrong, 1987). Teakle et al. (pp.…”

Role of Abscisic Acid in Flood-Induced Secondary Aerenchyma Formation in Soybean (Glycine max) Hypocotyls

“…Under flooded conditions, the phellogen also develops a homologous tissue, secondary aerenchyma, in the stems, roots, and root nodules in some plant species. Examples include some Fabaceae plants such as Sesbania aculeata (Scott and Wager, 1888), Sesbania rostrata (Saraswati et al, 1992;Shiba and Daimon, 2003), Neptunia oleracea (Metcalfe, 1931), Melilotus siculus (Teakle et al, 2011;Verboven et al, 2012), and Viminaria juncea (Walker et al, 1983). In addition, this phenomenon is observed in Onagraceae, e.g., Ludwigia spp.…”