Structural and photosynthetic re-acclimation to low light in C4 maize leaves that developed under high light

Abstract

Background and aims: C4 plants have higher photosynthetic capacity than C3 plants, but this advantage comes at an energetic cost that is problematic under low light. In the crop canopy, lower leaves first develop under high light but later experience low light because of mutual shading. To explore the re-acclimation of C4 leaves to low light, we investigated the structural and physiological changes of the leaves of maize plants grown in shaded pots.

Methods: Plants were first grown under high light, and then some of them were shaded (20 % of sunlight) for 3 weeks. Four types of leaves were examined: new leaves that developed under low light during shading (L), new leaves that developed under high light (H), mature leaves that developed under high light before shading and were then subjected to low light (H-L) and mature leaves that always experienced high light (H-H).

Key results: The leaf mass per area, nitrogen and chlorophyll contents per unit leaf area, chlorophyll a/b ratio and activities of C3 and C4 photosynthetic enzymes were lower in H-L than in H-H leaves and in L than in H leaves. Unlike L leaves, H-L leaves maintained the thickness and framework of the Kranz anatomy of H leaves, but chloroplast contents in H-L leaves were reduced. This reduction of chloroplast contents was achieved mainly by reducing the size of chloroplasts. Although grana of mesophyll chloroplasts were more developed in L leaves than in H leaves, there were no differences between H-L and H-H leaves. The light curves of photosynthesis in H-L and L leaves were very similar and showed traits of shade leaves.

Conclusions: Mature maize leaves that developed under high light re-acclimate to low-light environments by adjusting their biochemical traits and chloroplast contents to resemble shade leaves but maintain the anatomical framework of sun leaves.

Keywords: C4 plant; chloroplast; leaf structure; light re-acclimation; maize; photosynthetic traits; shade leaf; sun leaf.

Fig. 1.

Shading experiment for leaves of maize plants. Plants were first grown under high light and then grown for 3 weeks under cloths (shading treatment) or without cloths (control). An H leaf is a new leaf developed under high light. An L leaf is a new leaf developed under low light. An H–H leaf is a mature leaf first developed under high light and then exposed to high light for 3 weeks. An H–L leaf is a mature leaf first developed under high light and then exposed to low light for 3 weeks.

Fig. 2.

Response of net photosynthetic rate (P_N) to photon flux density (PFD) of maize plants. H, L, H–H and H–L have the same meaning as in Fig. 1. (A, B) Full light curves of P_N; (C, D) P_N at low irradiances. Means ± s.d. of 3–5 plants in each treatment. Significance at *P < 0.05; **P < 0.01; ***P < 0.001.

Fig. 3.

Transverse sections of upper and lower leaves of maize plants. (A) H leaf; (B) L leaf; (C) H–H leaf; (D) H–L leaf. BSC, bundle sheath cell; MC, mesophyll cell; V, vascular bundle. Scale bars = 50 μm.

Fig. 4.

Ultrastructure of bundle sheath chloroplasts in upper and lower leaves of maize plants. (A) H leaf. (B) L leaf. (C) H–H leaf. (D) H–L leaf. (E, F) Convoluted thylakoid structure of H–H and H–L leaves, respectively. Insets in (A) to (D) show enlarged images of thylakoids, and arrows show rudimentary grana. c, chloroplast; s, starch grain; SL, suberized lamella. Scale bars = 1 μm for (A–D), 0.5 μm for (E) and (F), and 0.25 μm for insets of (A–D).

Fig. 5.

Ultrastructure of mesophyll chloroplasts in upper and lower leaves of maize plants. (A) H leaf. (B) L leaf. (C) H–H leaf. (D) H–L leaf. c, chloroplast; g, granum; mt, mitochondrion. Scale bars = 1 μm.