Physiological roles for aerenchyma in phosphorus-stressed roots

Abstract

Low phosphorus availability induces the formation of cortical aerenchyma in roots. The adaptive significance of this response is unknown. We hypothesized that aerenchyma may be helpful to low-phosphorus plants by reducing root respiratory and phosphorus requirements, thereby increasing the metabolic efficiency of soil exploration. To test this hypothesis we investigated aerenchyma formation, root respiration and tissue phosphorus concentration in maize and common bean genotypes in response to phosphorus availability and ethylene treatments. Genotypes differed substantially in their ability to form aerenchyma in response to low phosphorus. Aerenchyma formation was disproportionately correlated with reduced root respiration; roots with 30% cross-sectional area as aerenchyma had 70% less respiration than roots without aerenchyma. Aerenchyma formation was also proportionally correlated with reduced root phosphorus concentration. Variation in aerenchyma formation was correlated with root respiration and phosphorus concentration, regardless of whether such variation was caused genetically or by ethylene or phosphorus treatments. Results with isolated roots were confirmed by measurement of whole root respiration of intact maize plants. Our results support the hypothesis that aerenchyma formation reduces the respiratory and phosphorus requirements of soil exploration by roots, and thus, represents a useful adaptation to low phosphorus availability.

Root Cortical Aerenchyma Enhances Nitrogen Acquisition from Low-Nitrogen Soils in Maize

“…N in lysed root tissue of high-RCA plants could be reabsorbed and utilized to support plant growth, as evidenced by greater root and shoot growth of high-RCA RILs compared with low-RCA RILs in low-N soils. These results are consistent with responses found under suboptimal availability of P and water (Fan et al, 2003;Zhu et al, 2010a). The results support our hypothesis that reduced root maintenance costs allow high-RCA RILs to support a larger root system and have greater soil exploration than low-RCA RILs.…”

“…3; Fan et al, 2003;Zhu et al, 2010a). Root respiration associated with growth, maintenance, and ion uptake are major components of root metabolic costs (Lambers et al, 1996;Lynch and Ho, 2005).…”

“…Several lines of evidence suggest that RCA enhances root metabolic efficiency under stress. Fan et al (2003) found that RCA formation significantly reduced root segment respiration and P content of root tissue, which allowed greater shoot growth in soils with low P availability. Under drought, maize genotypes with high RCA formation had greater root length, deeper rooting, better leaf water status, and 8 times greater yield than closely related genotypes with low RCA (Zhu et al, 2010a).…”

“…RCA is known to form in response to hypoxia, and the role of RCA in improving oxygen transport to roots of many plant species under hypoxic conditions has been well researched (Vartapetian and Jackson, 1997;Jackson and Armstrong, 1999;Omori, 2007, 2013). Interestingly, RCA can also form in response to drought and edaphic stresses such as N, P, and sulfur deficiencies (Drew et al, 1989;Bouranis et al, 2003;Fan et al, 2003;Zhu et al, 2010a), which suggests that the benefit of RCA extends beyond facilitating oxygen transport. Several lines of evidence suggest that RCA enhances root metabolic efficiency under stress.…”

Acclimation to soil flooding — sensing and signal-transduction

“…However, it is conceivable that the increased ethylene sensitivity of phosphorus-and nitrogen-depleted plants serves a different goal than aerenchyma formation per se, e.g., a change in root topology (Borch et al, 1999) or the formation of root hairs (although the latter is unlikely given the evidence provided by Schmidt and Schikora (2001) that low iron but not low phosphorus induces root hairs via the ethylene-perception pathway). On the other hand, Fan et al (2003) measured respiration rates of phosphorusstarved roots, which were lower per volume root due to the lower number of cells after aerenchyma developed. Combined with the assumption that cell components are being resorbed during cell lysis, this would imply a lower investment of construction and maintenance costs per unit root length, which would in turn add to the capacity of the plant to explore the soil for sources of phosphorous.…”