Han Dong, Jiachun Wang, Xuewei Song, +10 , and Jingquan Yu

PNAS April 10, 2023; 120 (16) e2301879120

https://doi.org/10.1073/pnas.230187912

Significance

The orchestration of shoot architecture, which is a major determinant of crop productivity, requires the regulated suppression or activation of -bud outgrowth. We show that light quality regulated tomato bud outgrowth is dependent on the mobile signaling protein HY5 and that HY5 dependent light signaling alone is sufficient to regulate bud outgrowth. HY5 promotes bud growth by direct and brassinosteroid mediated suppression of BRC1. BRC1 blocks the accumulation of cytokinin and gibberellin that regulate bud growth in tomato. In this way, HY5 represses gibberellin mediated stem elongation during photomorphogenesis while activating branching through BRC1 dependent phytohormone regulation. The HY5–BRC1 module thus plays predominant roles in the shoot architecture by orchestrating light quality dependent changes in stem elongation and bud outgrowth.

Abstract

Light plays an important role in determining plant architecture, which greatly influences crop yield. However, the precise mechanisms by which light signaling regulates bud outgrowth remain to be identified. Here, we show that light regulates bud outgrowth via both HY5 and brassinosteroid (BR)-dependent pathways in tomato. Inactivation of the red-light photoreceptor PHYB, or deficiencies in PHYB or the blue-light photoreceptor CRY1a, inhibits bud outgrowth and leads to decreased accumulation of HY5 protein and increased transcript level of BRANCHED1 (BRC1), a central integrator of branching signals. HY5, functioning as a mobile systemic signal from leaves, promotes bud outgrowth by directly suppressing BRC1 transcript and activating the transcript of BR biosynthesis genes within the lateral buds in tomato. Furthermore, BRC1 prevents the accumulation of cytokinin (CK) and gibberellin (GA) by directly inhibiting the transcript of CK synthesis gene LOG4, while increasing the transcript levels of CK and GA degradation genes (CKX7, GA2ox4, and GA2ox5), leading to an arrest of bud outgrowth. Moreover, bud outgrowth occurs predominantly in the day due to the suppression of BRC1 transcript by HY5. These findings demonstrate that light-inducible HY5 acts as a systemic signaling factor in fine-tuning the bud outgrowth of tomato.

See https://www.pnas.org/doi/10.1073/pnas.2301879120

Figure 1: Light regulates bud outgrowth via (BR)-dependent and -independent pathways in tomato. (A–C) Transcript of DET2 and DWF, BL level, and accumulation of BZR1 protein in the lateral buds in WT plants after exposure to different light regimes of R/FR ratio. (D and E) Bud outgrowth and transcript of BRC1 in the lateral buds of BR mutants after exposure to different light regimes of R/FR ratio. (F and G) Bud outgrowth and transcript of BRC1 in the lateral buds of photoreceptor mutants, WT and CRY1a-OE plants under WL. (H and I) The accumulation of HY5 protein in the lateral buds in WT plants after exposure to different light regimes of R/FR ratio and in the lateral buds of photoreceptor mutants, WT and  CRY1a-OE plants under WL. Samples were taken at 12 AM in G and I, or 6 h after the light quality treatment in A–C, E, and H. ACTIN2 and UBI3 were used as reference genes with the expression in WT as 1. Actin was used as a loading control for the western blot analysis. Data are presented as the means of replicates ± SD. n = 12 to 15 in D and F and n = 3 to 4 in A, B, E, and G. Different letters indicate significant differences (P < 0.05) according to Tukey’s test.