INTRODUCTION
The chloroplast is a complex cellular organelle that not only performs
photosynthesis but also synthesizes various macromolecules and
metabolites including fatty acids, vitamins, tetrapyrroles, and amino
acids required for plant growth (Allen, Paula, Puthiyaveetil, & Nield,
2011; Jarvis & Lopez-Juez, 2014). Chloroplasts contain their own DNA
and protein-synthesizing apparatus. Many key components of the
photosynthetic machinery are encoded by the chloroplast genome (Waters
& Langdale, 2009). Mitochondria, which are present in all eukaryotes,
are the site of cellular respiration that provides energy in the form of
ATP via oxidative phosphorylation for driving cellular metabolism.
Endo-symbiotic evolution within higher plants resulted in the emergence
of semi-autonomous organelles such as chloroplasts and mitochondria
(Rigas, Daras, Tsitsekian, Alatzas, & Hatzopoulos, 2014). Most
mitochondrial and chloroplast proteins are encoded by the nuclear
genome, expressed in the cytosol, and then imported into the organelles
(Yusuke et al., 2014). Although the nucleus regulates the development
and function of organelles, signals are also sent to the nucleus by
these organelles to deliver information regarding their growth and
developmental status to adjust the expression of nuclear genes (Nott,
Jung, Koussevitzky, & Chory, 2006). For example, COE1 andCOE2 , which play a role in plastid retrograde signaling, have a
significant impact on chloroplast biogenesis and plant growth (Sun, Xu,
Liu, Kleine, & Leister, 2016; Wu et al., 2022).
Retrograde signaling modulates nuclear gene expression in response to
changes in organellar status. Mitochondria and chloroplasts, the two
energy-converting organelles of plants, are closely coordinated to
balance their activity (Wang et al., 2020). Likewise, anterograde
signaling pathways control the expression of nuclear genes encoding
factors involved in plastid gene expression and tetrapyrrole
biosynthesis (Woodson & Chory, 2008). Plastids produce retrograde
signals to alter the expression of nuclear genes in response to
stress-related damage (Inaba, Yazu, Ito-Inaba, Kakizaki, & Nakayama,
2011). Developing chloroplasts in Arabidopsis thaliana are
vulnerable to photo-oxidative damage because they lack protective
carotenoids. This type of damage perturbs the tetrapyrrole biosynthetic
pathway resulting in the accumulation of several tetrapyrrole
intermediates and the down-regulation of PhANGs (Strand, Asami,
Alonso, Ecker, & Chory, 2003). Various genome-uncoupled(gun ) mutants in which this type of retrograde signaling is
impaired (e.g., gun1 – gun6 ) have been identified and
characterized in previous studies (Koussevitzky, 2007; Larkin, Alonso,
Ecker, & Chory, 2003; Mochizuki, Brusslan, Larkin, Nagatani, & Chory,
2001; Strand et al., 2003; Susek, Ausubel, & Chory, 1993; Woodson,
Perez-Ruiz, & Chory, 2011).
In plants, mitochondrial retrograde signaling is associated with
reactive oxygen species (ROS) signaling, pathogen sensing, and
programmed cell death (Rhoads & Subbaiah, 2007; Woodson & Chory,
2008). Some types of cytoplasmic male sterility in flowering plants are
induced by retrograde signaling in response to mitochondrial dysfunction
(Sota & Kinya, 2008). Calcium ion signaling, protein kinases, nuclear
TFs, and rare protein subunits have been shown to be involved in the
mitochondrial retrograde signaling pathway (Guha & Avadhani, 2013;
Guha, Srinivasan, Koenigstein, Zaidi, & Avadhani, 2016; Thierry,
Sébastien, & Patricia, 2015).
Chloroplasts and mitochondria are metabolically interdependent in the
photosynthetic cells of plants (Raghavendra & Padmasree, 2003). Carbon
dioxide (CO2) and ATP produced by the mitochondria are
used during photosynthesis, and the photosynthetic byproducts oxygen
(O2) and malate are used by the mitochondria.
Mitochondria also consume the redox products of chloroplasts and protect
them from damage caused by over-reduction of the photosynthetic electron
transport chain and photoinhibition (Raghavendra & Padmasree, 2003).
During photorespiration exchange of serine and glycine between
mitochondria and chloroplasts is mediated by peroxidases (Peter et al.,
2004).
In plant cells, ATP synthases are present in chloroplasts and
mitochondria. The mitochondrial ATP synthase, also known as F1Fo-ATP
synthase, catalyzes oxidative phosphorylation and uses the transmembrane
proton gradient to synthesize ATP (Stock, Leslie, & Walker, 1999).
Mitochondrial ATP synthase consists of two separate parts: F1 and Fo.
The F1 portion protrudes into the mitochondrial matrix and consists of
the a, b, g and d -subunits. The β -subunit carries
the catalytic site for ATP synthesis, and catalysis occurs through
highly coordinated conformational changes in the α andβ -subunits (Xu, Pagadala, & Mueller, 2015). Fo acts as a turbine
driven by proton flow and is inserted in the inner membrane and linked
to the F1 rotor.
The C-terminal domain of the β -subunit consists of a highly
conserved helix-turn-helix motif termed “DELSEED-loop,” likely to be
involved in the coupling between catalysis and rotation (Mnatsakanyan,
Krishnakumar, Suzuki, & Weber, 2009). Loss of the 10 residues of the
DELSEED-loop abolishes ATP synthesis (Mnatsakanyan, Kemboi, Salas, &
Weber, 2011).
Low levels of ATP are sensed by SnRK1 which phosphorylates the SOG1
protein, thereby increasing the expression of cell cycle-related genes
(cyclin-dependent protein kinase 3 ;2, CYCA3 ;2 orcyclin D-type protein 3;3 , CYCD3;3 ) to inhibit plant cell
growth (Hamasaki et al., 2019).
Here, we studied a mutant affected in AT5G08670 encoding the
mitochondrial ATP synthaseβ- subunit which leads to a
decrease in ATP synthase level and activity. Transcriptome analysis
revealed that the transcriptome profile of this mutant is significantly
altered compared to the wild type. The expression of chloroplast and
mitochondrial retrograde signaling-related genes and some TFs are
affected in the mutant treated with LIN, an inhibitor of chloroplast
protein synthesis. These results indicate that mitochondrial ATP levels
affect plastid retrograde signaling.