Cytochrome c and the transcription factor ABI4 establish a molecular link between mitochondria and ABA‐dependent seed germination

Abstract

During germination, seed reserves are mobilised to sustain the metabolic and energetic demands of plant growth. Mitochondrial respiration is presumably required to drive germination in several species, but only recently its role in this process has begun to be elucidated.Using Arabidopsis thaliana lines with changes in the levels of the respiratory chain component cytochrome c (CYTc), we investigated the role of this protein in germination and its relationship with hormonal pathways.Cytochrome c deficiency causes delayed seed germination, which correlates with decreased cyanide-sensitive respiration and ATP production at the onset of germination. In addition, CYTc affects the sensitivity of germination to abscisic acid (ABA), which negatively regulates the expression of CYTC-2, one of two CYTc-encoding genes in Arabidopsis. CYTC-2 acts downstream of the transcription factor ABSCISIC ACID INSENSITIVE 4 (ABI4), which binds to a region of the CYTC-2 promoter required for repression by ABA and regulates its expression.The results show that CYTc is a main player during seed germination through its role in respiratory metabolism and energy production. In addition, the direct regulation of CYTC-2 by ABI4 and its effect on ABA-responsive germination establishes a link between mitochondrial and hormonal functions during this process.

Cytochrome c levels affect the TOR pathway to regulate growth and metabolism under energy‐deficient conditions

“…Plants with decreased CYTc levels have shorter roots, reduced growth in the presence of sugars, and altered energy metabolism Previous reports showed that cytc double mutant plants with lower CYTc levels (cytc-1b2a and cytc-1b2b) exhibited delayed New Phytologist germination and developmental growth transitions (Racca et al, 2018(Racca et al, , 2022. Since effects on postgerminative growth were mainly attributed to the activity of CYTC-1, one of the two genes encoding CYTc in Arabidopsis thaliana, we analyzed the phenotypic characteristics of cytc-1 single mutant plants (cytc-1a and cytc-1b), previously described in Welchen et al (2012).…”

“…We previously reported that, while a complete CYTc deficiency is embryo lethal, double mutants in both CYTC genes from Arabidopsis (knock‐down in CYTC‐1 and knock‐out in CYTC‐2 ) show growth defects, including delayed germination and developmental transitions, but are able to complete their life cycle and efficiently reproduce (Welchen et al ., 2012; Racca et al ., 2018, 2022). Here, we found that cytc‐1 single mutant seedlings (Fig.…”

“…Our previous research suggests that CYTc levels play a crucial role in plant growth, as its deficiency and overexpression significantly affect plant growth rate (Welchen et al, 2012;Racca et al, 2018Racca et al, , 2022. To examine a possible connection between CYTc and the TOR pathway, we analyzed CYTc protein levels in plants affected by different components of this pathway.…”

“…Thus, altered CYTc expression impacts the activity of abscisic acid (ABA) and gibberellin-regulated pathways during germination and vegetative growth, respectively. Plants with reduced CYTc levels have delayed germination and lower levels of GAs-content that are traduced in a delayed developmental transition during vegetative and reproductive life stages (Racca et al, 2018(Racca et al, , 2022.…”

“…Previously, we reported that a complete CYTc deficiency leads to embryo lethality (Welchen et al, 2012). Arabidopsis plants with reduced expression of both genes encoding CYTcknockdown for CYTC-1 (At1g22840) and knockout for CYTC-2 (At4g10040)show growth defects, including delayed germination and developmental transitions (Racca et al, 2018(Racca et al, , 2022. In this work, we describe that the alterations observed in CYTc-deficient plants are related to changes in the TOR-pathway activity, hinting at the existence of a mitochondrial signal to adjust growth and metabolism according to energy availability to avoid affecting essential cellular processes under nonoptimal energetic conditions.…”