Asymmetric auxin distribution establishes a contrasting pattern of aerenchyma formation in the nodal roots of Zea nicaraguensis during gravistimulation.

Auxin distribution is essential for determining root developmental patterns. The formation of lateral roots and constitutive aerenchyma, which is a gas space developed through cell death, is regulated by auxin in rice (Oryza sativa). However, it is unclear whether the involvement of auxin in constitutive aerenchyma formation is conserved in other species. In this study, we found that constitutive aerenchyma formation was regulated by auxin in the nodal roots of Zea nicaraguensis, a wild relative of maize (Zea mays ssp. mays) grown naturally on frequently flooded coastal plains. Subsequent gravistimulation (root rotation) experiments showed opposite patterns of aerenchyma and lateral root formation. Lateral root formation on the convex side of rotated roots is known to be stimulated by a transient increase in auxin level in the pericycle. We found that aerenchyma formation was accelerated in the cortex on the concave side of the rotated nodal roots of Z. nicaraguensis. A cortex-specific expression analysis of auxin-responsive genes suggested that the auxin level was higher on the concave side than on the convex side. These results suggest that asymmetric auxin distribution underlies the regulation of aerenchyma and lateral root formation in the nodal roots of Z. nicaraguensis. As aerenchyma reduces the respiratory cost of the roots, constitutive aerenchyma on the concave side of the nodal root may balance resource allocation, thereby contributing to the uptake of water and nutrients by newly formed lateral roots. Our study provides insights into auxin-dependent asymmetric root patterning such as that of gravistimulation and hydropatterning response.

Lateral roots, in addition to adventitious roots, form a barrier to radial oxygen loss in Zea nicaraguensis and a chromosome segment introgression line in maize.

Plants typically respond to waterlogging by producing new adventitious roots with aerenchyma and many wetland plants form a root barrier to radial O2 loss (ROL), but it was not known if this was also the case for lateral roots. We tested the hypothesis that lateral roots arising from adventitious roots can form a ROL barrier, using root-sleeving electrodes and O2 microsensors to assess ROL of Zea nicaraguensis, the maize (Zea mays ssp. mays) introgression line with a locus for ROL barrier formation (introgression line (IL) #468) from Z. nicaraguensis and a maize inbred line (Mi29). Lateral roots of Z. nicaraguensis and IL #468 both formed a ROL barrier under stagnant, deoxygenated conditions, whereas Mi29 did not. Lateral roots of Z. nicaraguensis had higher tissue O2 status than for IL #468 and Mi29. The ROL barrier was visible as suberin in the root hypodermis/exodermis. Modelling showed that laterals roots can grow to a maximum length of 74 mm with a ROL barrier, but only to 33 mm without a barrier. Presence of a ROL barrier in lateral roots requires reconsideration of the role of these roots as sites of O2 loss, which for some species now appears to be less than hitherto thought.

QTLs for constitutive aerenchyma from Zea nicaraguensis improve tolerance of maize to root-zone oxygen deficiency.

Zea nicaraguensis is a wild relative of Zea mays subsp. mays (maize) that has high waterlogging tolerance. One of its traits is constitutive aerenchyma formation (CAF) in roots and this may be one of the reasons for the tolerance, but it has not yet been proven by comparing plants that differ only in CAF in the same genetic background. We therefore produced an introgression line AE24-50-44-91 (IL-AE91) possessing four quantitative trait loci for CAF from Z. nicaraguensis in the background of maize (inbred line Mi29). The degree of root CAF in IL-AE91 was intermediate between that of Mi29 and Z. nicaraguensis. Seedlings of IL-AE91 grown aerobically were more tolerant to transfer to oxygen-deficient conditions than were Mi29 seedlings. On day 2 of oxygen deficiency, the root extension rate and viability of root-tip cells in IL-AE91 were ~2.7 and ~1.3 times greater, respectively, than they were in Mi29. On day 4, the area of aerenchyma at 80 mm from the root tips was ~1.5 times greater in IL-AE91 and radial oxygen loss from the apical parts of roots was ~3.4 times higher than in Mi29. These results demonstrate that CAF reduces the stress from low external oxygen levels caused by soil waterlogging.

A major locus involved in the formation of the radial oxygen loss barrier in adventitious roots of teosinte Zea nicaraguensis is located on the short-arm of chromosome 3.

A radial oxygen loss (ROL) barrier in roots of waterlogging-tolerant plants promotes oxygen movement via aerenchyma to the root tip, and impedes soil phytotoxin entry. The molecular mechanism and genetic regulation of ROL barrier formation are largely unknown. Zea nicaraguensis, a waterlogging-tolerant wild relative of maize (Zea mays ssp. mays), forms a tight ROL barrier in its roots when waterlogged. We used Z. nicaraguensis chromosome segment introgression lines (ILs) in maize (inbred line Mi29) to elucidate the chromosomal region involved in regulating root ROL barrier formation. A segment of the short-arm of chromosome 3 of Z. nicaraguensis conferred ROL barrier formation in the genetic background of maize. This chromosome segment also decreased apoplastic solute permeability across the hypodermis/exodermis. However, the IL and maize were similar for suberin staining in the hypodermis/exodermis at 40 mm and further behind the root tip. Z. nicaraguensis contained suberin in the hypodermis/exodermis at 20 mm and lignin at the epidermis. The IL with ROL barrier, however, did not contain lignin in the epidermis. Discovery of the Z. nicaraguensis chromosomal region responsible for root ROL barrier formation has improved knowledge of this trait and is an important step towards improvement of waterlogging tolerance in maize.