Associations between the acclimation of phloem-cell wall ingrowths in minor veins and maximal photosynthesis rate

Abstract

The companion cells (CCs) and/or phloem parenchyma cells (PCs) in foliar minor veins of some species exhibit invaginations that are amplified when plants develop in high light (HL) compared to low light (LL). Leaves of plants that develop under HL also exhibit greater maximal rates of photosynthesis compared to those that develop under LL, suggesting that the increased membrane area of CCs and PCs of HL-acclimated leaves may provide for greater levels of transport proteins facilitating enhanced sugar export. Furthermore, the degree of wall invagination in PCs (Arabidopsis thaliana) or CCs (pea) of fully expanded LL-acclimated leaves increased to the same level as that present in HL-acclimated leaves 7 days following transfer to HL, and maximal photosynthesis rates of transferred leaves of both species likewise increased to the same level as in HL-acclimated leaves. In contrast, transfer of Senecio vulgaris from LL to HL resulted in increased wall invagination in CCs, but not PCs, and such leaves furthermore exhibited only partial upregulation of photosynthetic capacity following LL to HL transfer. Moreover, a significant linear relationship existed between the level of cell wall ingrowths and maximal photosynthesis rates across all three species and growth light regimes. A positive linear relationship between these two parameters was also present for two ecotypes (Sweden, Italy) of the winter annual A. thaliana in response to growth at different temperatures, with significantly greater levels of PC wall ingrowths and higher rates of photosynthesis in leaves that developed at cooler versus warmer temperatures. Treatment of LL-acclimated plants with the stress hormone methyl jasmonate also resulted in increased levels of wall ingrowths in PCs of A. thaliana and S. vulgaris but not in CCs of pea and S. vulgaris. The possible role of PC wall ingrowths in sugar export versus as physical barriers to the movement of pathogens warrants further attention.

Keywords: biotic defense; companion cells; leaf vasculature; light acclimation; phloem; photosynthesis; temperature acclimation; transfer cells.

FIGURE 1

(A,C,E) Foliar light- and CO₂-saturated rate of photosynthetic oxygen evolution ascertained at 25°C and (B,D,F) percent increase in plasma membrane length due to cell wall ingrowths estimated from cross-sections of phloem transfer cells (parenchyma = PC, companion = CC) relative to the hypothetical membrane area in the absence of wall ingrowths in foliar minor veins of Italian (A,B), pea (C,D), and S. vulgaris (E,F) that developed in low light (LL), high light (HL), or LL and then transferred to HL for seven days. Light-gray columns indicate PCs and black-filled columns indicate CCs. Significant differences between means (P < 0.05) within each species are denoted by different lower-case letters, with the exception that upper-case letters are used to designate significant differences among the level of cell wall ingrowths for CCs, i.e., means sharing a common letter are not statistically different from each other. Photosynthetic capacities for pea from Amiard et al. (2005) and for A. thaliana and S. vulgaris grown in HL from Amiard et al. (2007).

FIGURE 2

Relationship between the percent increase of transfer-cell plasma membrane length in foliar minor veins and photosynthetic capacity from leaves of A. thaliana (light gray), pea (black), and S. vulgaris (dark gray) developed under LL or HL, or seven days after transfer of leaves developed under LL to HL. For S. vulgaris, the values for percent increase in transfer-cell plasma membrane length are averages of the mean values obtained from PCs and CCs. For additional information, see Figure 1.

FIGURE 3

Representative transmission electron-micrographic cross-sectional images of sieve elements (SE) surrounded by parenchyma (PC) and companion (CC) cells in foliar minor veins of Italian (A,B) or Swedish (C,D) ecotypes of A. thaliana that developed under 400 μmol photons m^–2s^–1 at a daytime leaf temperature of 36°C (A,C) or 14°C (B,D). Cell-wall ingrowths (WI) in the PCs are adjacent to the area abutting a neighboring SE, sometimes extend over the area of adjacent CCs (particularly apparent at lower temperature), and are more pronounced (greater level of invagination) in both ecotypes that developed at lower temperature. Black bar = 500 nm in length.

FIGURE 4

(A,C) Foliar light- and CO₂-saturated rate of photosynthetic oxygen evolution ascertained at 25°C and (B,D) percent increase in plasma-membrane length due to cell-wall ingrowths estimated from cross-sections of phloem-parenchyma transfer cells relative to the hypothetical membrane area in the absence of wall ingrowths in foliar minor veins of Italian (A,B) and Swedish (C,D) ecotypes of A. thaliana that developed under 400 μmol photons m^-2s^-1 at daytime leaf temperatures of 36 or 14°C. Significant differences between the means within each ecotype are denoted by asterisks (*P < 0.05, **P < 0.01, and ***P < 0.001). Photosynthetic capacities from leaves that developed at 14°C from Cohu et al. (2013b).

FIGURE 5

Relationship between the percent increase of parenchyma-cell plasma-membrane length in foliar minor veins and photosynthetic capacity from leaves of Italian (circles) or Swedish (triangles) ecotypes of A. thaliana that developed under 400 μmol photons m^–2s^–1 at a daytime leaf temperature of 36°C (lowest values), 18°C (intermediate values), or 14°C (highest values). The linear relationship among all six values (not shown) was significant at P <0.05, whereas the linear relationships shown for each ecotype were not. Photosynthetic capacities from leaves that developed at 14°C from Cohu et al. (2013b).

FIGURE 6

Percent increase in plasma-membrane length due to cell-wall ingrowths estimated from cross-sections of phloem transfer cells (parenchyma = PC, companion = CC) relative to the hypothetical membrane area in the absence of wall ingrowths in foliar minor veins of A. thaliana(A), pea (B), and S. vulgaris(C) that developed in low light and were sprayed with a 0.05% solution of Tween (LL) or a 0.05% solution of Tween with 10 μM methyl jasmonate (LL+MeJA) for seven days. Gray columns indicate PCs and black columns indicate CCs. Significant differences between the means (P <0.05) of A. thaliana (A) and S. vulgaris (C) are denoted by different lower case letters. Percent increase of plasma membrane length was not significantly different (n.s.) between control and MeJA-treated companion cells of either pea (B) or S. vulgaris (C). Data from Amiard et al. (2007).