Systemic induction of photosynthesis via illumination of the shoot apex is mediated by phytochrome B

Abstract

Systemic signaling of upper leaves promotes the induction of photosynthesis in lower leaves, allowing more efficient use of light flecks. However, the nature of the systemic signals has remained elusive. Here, we show that preillumination of the tomato (Solanum lycopersicum) shoot apex alone can accelerate photosynthetic induction in distal leaves and that this process is light quality dependent, where red light promotes and far-red light delays photosynthetic induction. Grafting the wild-type rootstock with a phytochome B (phyB) mutant scion compromised light-induced photosynthetic induction as well as auxin biosynthesis in the shoot apex, auxin signaling, and RESPIRATORY BURST OXIDASE HOMOLOG1 (RBOH1)-dependent hydrogen peroxide (H 2 O 2 ) production in the systemic leaves. Light-induced systemic H 2 O 2 production in the leaves of the rootstock also was absent in plants grafted with an auxin-resistant diageotropica (dgt) mutant scion. Cyclic electron flow around photosystem I and associated ATP production were increased in the systemic leaves by exposure of the apex to red light. This enhancement was compromised in the systemic leaves of the wild-type rootstock with phyB and dgt mutant scions and also in RBOH1-RNA interference leaves with the wild type as scion. Silencing of ORANGE RIPENING, which encodes NAD(P)H dehydrogenase, compromised the systemic induction of photosynthesis. Taken together, these results demonstrate that exposure to red light triggers phyB-mediated auxin synthesis in the apex, leading to H 2 O 2 generation in systemic leaves. Enhanced H 2 O 2 levels in turn activate cyclic electron flow and ATP production, leading to a faster induction of photosynthetic CO 2 assimilation in the systemic leaves, allowing plants better adaptation to the changing light environment.

A novel CO2‐responsive systemic signaling pathway controlling plant mycorrhizal symbiosis

“…For the analysis of indole‐3‐acetic acid (IAA), the developing leaves at the apex were used. IAA extraction and quantification were performed as described previously (Guo et al ., ). For the determination of SLs in the roots, 0.5 g of roots was blended in a blender at top speed for 1 min in 40% acetone (1 : 5, w / v ).…”

Light‐induced systemic signalling down‐regulates photosynthetic performance of soybean leaves with different directional effects

“…A similar situation was also found in another study on tomato ( Solanum lycopersicum L.), where the roles of cyclic electron flow and ATP production were indicated (Guo et al . ). Since exposure for several minutes is too short a time to influence the growth of leaves, the above results suggest that photosynthesis of leaves exhibited a clear response to light‐induced systemic signalling before morphological and structural changes occurred.…”

“…; Guo et al . ). Therefore, it seems that the effects of systemic regulation face practical obstacles in altering the photosynthesis level of a plant over such a short time, but the effects can be seen at the stage of photosynthetic induction.…”

Rapid systemic signaling during abiotic and biotic stresses: is the ROS wave master of all trades?

“…from the root to the shoot, or from lower leaves to upper leaves) or the downward (e.g. from the shoot to the root, or from upper leaves and/or flowering buds to lower leaves) direction (Suzuki et al , ; Gilroy et al , ; Gilroy et al , ; Guo et al , ; Choudhury et al , ; Lai et al , ; Wang et al , ; Zhou et al , ).…”