New insights into trophic aerenchyma formation strategy in maize (Zea mays L.) organs during sulfate deprivation

Abstract

Aerenchyma attributes plant tissues that contain enlarged spaces exceeding those commonly found as intracellular spaces. It is known that sulfur (S) deficiency leads to formation of aerenchyma in maize adventitious roots by lysis of cortical cells. Seven-day-old maize plants were grown in a hydroponics setup for 19 days under S deprivation against full nutrition. At day 17 and 26 from sowing (d10 and d19 of the deprivation, respectively), a detailed analysis of the total sulfur and sulfate allocation among organs as well as a morphometric characterization were performed. Apart from roots, in S-deprived plants aerenchyma formation was additionally found in the second leaf and in the mesocotyl, too. The lamina (LA) of this leaf showed enlarged gas spaces between the intermediate and small vascular bundles by lysis of mesophyll cells and to a greater extent on the d10 compared to d19. Aerenchymatous spaces were mainly distributed along the middle region of leaf axis. At d10, -S leaves invested less dry mass with more surface area, whilst lesser dry mass was invested per unit surface area in -S LAs. In the mesocotyl, aerenchyma was located near the scutelar node, where mesocotyl roots were developing. In -S roots, more dry mass was invested per unit length. Our data suggest that trying to utilize the available scarce sulfur in an optimal way, the S-deprived plant fine tunes the existing roots with the same length or leaves with more surface area per unit of dry mass. Aerenchyma was not found in the scutelar node and the bases of the attached roots. The sheaths, the LAs' bases and the crown did not form aerenchyma. This trophic aerenchyma is a localized one, presumably to support new developing tissues nearby, by induced cell death and recycling of the released material. Reduced sulfur allocation among organs followed that of dry mass in a proportional fashion.

Keywords: aerenchyma; deficiency; leaf; maize; mesocotyl; sulfate deprivation.

FIGURE 1

Cross sections taken from the second lamina (LA) of plants under full nutrition (C ) or S-deprivation (-S), at d10 and d19 of the treatment. A, the LA’s apex; M, middle; or B, base.

FIGURE 2

Cross sections taken from the middle of the second LA’s axis, that depict the three variations of aerenchyma connecting epidermis to epidermis (A), stoma to stoma (B), or stoma to epidermis (C).

FIGURE 3

Correlations of leaves’ dry mass (A,B), specific surface area (SSA; C,D), or accumulated amount of organic sulfur (Sorg; E,F) with the corresponding surface area. Each point respresents a leaf (sheath + lamina) and each value has been expressed per leaf. Full circle and bold line, control treatment; open circle and thin line: S-deprivation. Arrow indicates the corresponding y-axis.

FIGURE 4

Aerenchyma formation in mesocotyl near the scutelar node, at d10 and d19 of the sulfate deprivation (-S) and control (C) treatment.

FIGURE 5

Correlation of roots’ dry mass (A,D,G,J), specific root length (SRL; B,E,H,K) or accumulated amount of organic sulfur (Sorg; C,F,I,L) with the corresponding total length of each root type. Each point represents a root type (PR, primary root; SR, seminal roots; MR, mesocotyl roots; CR, crown roots) and each value has been expressed per organ. Full circle and bold line, control treatment; open circle and thin line: S-deprivation.

FIGURE 6

The relationship between the dry mass of each organ and the corresponding amount of organic sulfur at days 0, 10, and 19 of the treatment. Full circle and bold line, control treatment, open circle and thin line, S-deprivation treatment; At d19, the regression line of -S treatment represents only the points that followed the power function relationship (see text for Discussion). The arrow indicates the corresponding axis.