Cold-induced inhibition of photosynthesis-related genes integrated by a TOP6 complex in rice mesophyll cells

Abstract

Photosynthesis is the most temperature-sensitive process in the plant kingdom, but how the photosynthetic pathway responds during low-temperature exposure remains unclear. Herein, cold stress (4°C) induced widespread damage in the form DNA double-stranded breaks (DSBs) in the mesophyll cells of rice (Oryza sativa), subsequently causing a global inhibition of photosynthetic carbon metabolism (PCM) gene expression. Topoisomerase genes TOP6A3 and TOP6B were induced at 4°C and their encoded proteins formed a complex in the nucleus. TOP6A3 directly interacted with KU70 to inhibit its binding to cold-induced DSBs, which was facilitated by TOP6B, finally blocking the loading of LIG4, a component of the classic non-homologous end joining (c-NHEJ) pathway. The repression of c-NHEJ repair imposed by cold extended DSB damage signaling, thus prolonging the inhibition of photosynthesis in leaves. Furthermore, the TOP6 complex negatively regulated 13 crucial PCM genes by directly binding to their proximal promoter regions. Phenotypically, TOP6A3 overexpression exacerbated the γ-irradiation-triggered suppression of PCM genes and led to the hypersensitivity of photosynthesis parameters to cold stress, dependent on the DSB signal transducer ATM. Globally, the TOP6 complex acts as a signal integrator to control PCM gene expression and synchronize cold-induced photosynthesis inhibition, which modulates carbon assimilation rates immediately in response to changes in ambient temperature.

Transcriptome analyses reveal photosynthesis-related genes involved in photosynthetic regulation under low temperature stress in Lavandula angustifolia Mill.

“…Some ways in which low temperature interferes with photosynthesis mainly including the disruption of the photosynthetic pigment complex system and the membrane fluidity, the reduction of the photochemical efficiency of plant photosystems (PSI and PSII), the decrease in enzymatic activities, and the changes in electron transfer rate in thylakoid and metabolic processes (Özdemir et al, 2023;Xu et al, 2023). Moreover, low temperature brought photodamage of the PSII reaction center (Velitchkova et al, 2023), altered the light-harvesting antenna system and reaction center structure, disrupted the photosynthetic structure (Sachdev et al, 2023), and caused inhibition of photosynthesis (Zhang et al, 2023), which decreased the photosynthetic capacity (Guo et al, 2023).…”

Effect of gibberellic acid on photosynthesis and oxidative stress response in maize under weak light conditions

“…The template comprised cDNA diluted 20 times and it was repeated three times. The total reaction system volume was 20 μL and the reaction conditions comprised: 95°CC for 30 s, and 45 cycles at 60°CC for 30 s and 72°CC for 30s ( Xu et al., 2023 ). After PCR, the dissolution curve was analyzed.…”

The Molecular Mechanism of Cold-Stress Tolerance: Cold Responsive Genes and Their Mechanisms in Rice (Oryza sativa L.)

“…The modulation of gene expression in response to cold stress in rice plants mainly involves the genes associated with stress response, metabolism, and signal transduction pathways, especially plant hormones metabolism and signal transduction [ 23 ]. When exposed to cold stress, the level of ABA in plants is observed to increase significantly, which subsequently enhances endogenous defense mechanisms.…”