MITOCH-00908; No of Pages 8 Mitochondrion xxx (2014) xxx–xxx

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Mitochondrial biogenesis in plants during seed germination Simon R. Law a, Reena Narsai b, James Whelan b,⁎ a b

Australian Research Council Centre of Excellence in Plant Energy Biology, University of Western Australia, 35 Stirling Highway, Crawley, Western Australia, 6009, Australia Department of Botany, Australian Research Council Centre of Excellence in Plant Energy Biology, School of Life Science, La Trobe University, Bundoora, Victoria, 3086, Australia

a r t i c l e

i n f o

Article history: Received 9 February 2014 received in revised form 29 March 2014 accepted 1 April 2014 Available online xxxx Keywords: Seed germination Biogenesis Promitochondrion Signalling Stress Retrograde

a b s t r a c t Mitochondria occupy a central role in the eukaryotic cell. In addition to being major sources of cellular energy, mitochondria are also involved in a diverse range of functions including signalling, the synthesis of many essential organic compounds and a role in programmed cell death. The active proliferation and differentiation of mitochondria is termed mitochondrial biogenesis and necessitates the coordinated communication of mitochondrial status within an integrated cellular network. Two models of mitochondrial biogenesis have been defined previously, the growth and division model and the maturation model. The former describes the growth and division of pre-existing mature organelles through a form of binary fission, while the latter describes the propagation of mitochondria from structurally and biochemically simple promitochondrial structures that upon appropriate stimuli, mature into fully functional mitochondria. In the last decade, a number of studies have utilised seed germination in plants as a platform for the examination of the processes occurring during mitochondrial biogenesis. These studies have revealed many new aspects of the tightly regulated procession of events that define mitochondrial biogenesis during this period of rapid development. A model for mitochondrial biogenesis that supports the maturation of mitochondria from promitochondrial structures has emerged, where mitochondrial signalling plays a crucial role in the early steps of seed germination. © 2014 Elsevier B.V. and Mitochondria Research Society. All rights reserved.

1. Introduction The defining feature of the eukaryotic cell is the compartmental organisation of the cellular landscape compared to the relatively simpler structure of prokaryotic cells. While traditional hypotheses of the origin of mitochondria suggest an endosymbiotic event with a nucleated cell, no evidence for such a cellular organism exists. In fact, eukaryotic cells that lack ‘true’ mitochondria, such as Giardia and trichomonads that contain mitosomes and hydrogensomes, respectively, are now recognised to represent a subsequent loss of mitochondria, with these organelles derived from the same endosymbiotic ancestor (Henze and Martin, 2003). Recent observations suggest that it may have been the mitochondrial endosymbiotic event itself that prompted the formation of internal membrane structures of the cell, including the formation of the nucleus (Lane and Martin, 2010). In light of this, the central signalling and controlling role of the nucleus may not be as predominant as is widely believed, and recent studies reveal crucial roles for the mitochondrion in many processes, beyond that of the traditional metabolic organelle. Mitochondria occupy many roles in the cellular landscape, including (1) the synthesis of vitamins such as ascorbic acid, folic acid and biotin and selected amino acids (Birke et al., 2012; Rebeille et al., 2007); (2) being a major site of ROS production and thus having ⁎ Corresponding author. Tel.: +61 3 90327488. E-mail address: [email protected] (J. Whelan).

a role in cellular signalling (Rhoads et al., 2006); (3) as active participants in various metabolic and physiological pathways such as nitrogen assimilation (Foyer et al., 2011), iron homeostasis (Jain and Connolly, 2013) and lipid metabolism (Baker et al., 2006); (4) playing a central role in programmed cell death (PCD) (Reape and McCabe, 2010); and (5) producing cellular energy in the form of ATP through oxidative phosphorylation (Lenaz and Genova, 2010). As a vestige of their endosymbiotic origin, mitochondria possess their own genome. Over time, significant portions of this genome have been lost or transferred to the host nucleus, where it was free to recombine with host DNA (Martin et al., 1993). Consequently, mitochondria are unable to arise de novo in the manner of other organelles such as peroxisomes, endoplasmic reticulum (ER) and Golgi apparatus. Instead, two models have been hypothesised to explain their proliferation and differentiation; termed mitochondrial biogenesis (Nisoli et al., 2004). The first proposes the growth and division of pre-existing mature organelles through a form of binary fission that betrays their bacterial ancestry, while the second posits that mature organelles develop from small and functionally simple precursor organelles, termed promitochondria (Nisoli et al., 2004). Mitochondrial biogenesis is a tightly regulated and multi-step procedure that requires the careful coordination of many processes, such as DNA replication, transcription, RNA modification (e.g., editing and splicing), translation and protein translocation, in addition to synchronising protein complex assembly with subunits from nuclear and mitochondrial origins (Chacinska et al., 2008; Giege et al., 2005; McCabe et al.,

http://dx.doi.org/10.1016/j.mito.2014.04.002 1567-7249/© 2014 Elsevier B.V. and Mitochondria Research Society. All rights reserved.

Please cite this article as: Law, S.R., et al., Mitochondrial biogenesis in plants during seed germination, Mitochondrion (2014), http://dx.doi.org/ 10.1016/j.mito.2014.04.002

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2000; Menassa et al., 1999; Zmudjak et al., 2013). The literature describing the growth and division model of mitochondrial biogenesis has been established for many years from studies in Saccharomyces cerevisiae (yeast) and mammalian systems (Grivell, 1989; Nisoli et al., 2004; Tzagoloff and Myers, 1986). It has been shown that mitochondrial fission generally coincides with mitosis, with mitochondrial mass increasing during the period from S-phase to M-phase, ensuring that the resulting daughter cells receive a roughly equal complement of mitochondria upon cellular fission (Jahnke et al., 2009; Sanger et al., 2000). The second model of mitochondrial biogenesis, termed the maturation model, is not as well understood or studied. Initially observed in yeast systems, it describes the maturation of pre-existing populations of structurally and metabolically simple organelles, termed promitochondria, which develop into metabolically active ‘mature’ mitochondria. Specifically, populations of these promitochondria, with a deficient respiratory potential, were identified in yeast cells grown under anaerobic conditions, which were able to regain the ability to respire aerobically upon aeration (Plattner et al., 1970). A more recent study incorporated electron microscopy to define the ultrastructure of these precursor structures during the transition into mature mitochondria (Rosenfeld et al., 2004). The available evidence suggests that, unlike the growth and division model, which occurs far more frequently and under many different conditions, the maturation model is restricted to systems undergoing a fundamental phase transition, for example, yeast populations transitioning from anaerobic to aerobic conditions, or systems progressing from a state of quiescence to active metabolism, such as that seen during seed germination in plants. 2. Mitochondrial biogenesis during seed germination 2.1. Heterogeneity of mitochondrial populations in germinating seeds Seed germination represents an attractive system to study mitochondrial biogenesis, as it is a unique stage in the plant life cycle that is characterised by an extended period of quiescence, followed by a switch to an energetically demanding state that necessitates the rapid and synchronised production of mitochondria. Accordingly, seed germination has been utilised in a number of studies examining mitochondrial biogenesis in both monocot and dicot plant species (Dai et al., 1998; Howell et al., 2006; Law et al., 2012; Logan et al., 2001). In maize and rice, electron microscopy and proteomic analysis in dry and imbibing seedlings characterised a population of promitochondria with poorly developed internal membranes lacking cristae significantly deficient in components of the electron transport chain. In maize, sucrose density gradients were used to fractionate crude homogenates of embryos dissected from dry seeds and seeds at four time points following imbibition, which identified the presence of two distinct subpopulations of mitochondria (referred to as heavy and light mitochondria) at every time point assayed (Logan et al., 2001). In dry seed, both subpopulations were composed of poorly developed mitochondria with light mitochondria exhibiting no significant changes in membrane morphology or protein content throughout the time course. However, upon continued imbibition, heavy mitochondria were observed to take on the characteristic appearance of mature mitochondria, with numerous cristae structures and an electron dense matrix, suggestive of a higher protein content (Logan et al., 2001). In rice, it was observed that promitochondria isolated from dry seeds were unable to import proteins, despite being relatively enriched in proteins with biogenesis functions such as the mitochondrial protein import components (Howell et al., 2006). However, just 30 min of imbibition was sufficient to restore import capacity, with significant protein import rates detected in isolated mitochondria (Howell et al., 2007). This suggests that all the necessary machinery for protein import is present in dry seeds and is rapidly activated upon imbibition. As germination progressed, the protein abundance of mitochondrial import components was observed to decrease, while proteins associated with primary metabolism increased in abundance (Howell et al., 2006). Paradoxically, protein

import rates also increase over germination, while the abundance of the protein import machinery declines (Howell et al., 2006, 2007). This suggests that there may be some active degradation of the import machinery as the population shifts from promitochondria to mature mitochondria. 2.2. Which comes first, the mitochondrion or the promitochondrion? Little is known about the formation of promitochondrial structures. There is some speculation that they derive from the selective degeneration of mature, metabolically active mitochondria, akin to the dedifferentiation of chloroplasts into non-photosynthesising proplastids, observed at the end of the seed maturation phase (Allorent et al., 2013). It is during these final stages of maturation that the seed can lose as much as 95% of its water content, transforming the seed into an incredibly resilient structure capable of tolerating extended periods of debilitating conditions. During this time, cells become a highly hostile environment for membrane bound structures such as mitochondria (Manfre et al., 2009). To circumvent cellular damage that can result from an anhydrobiotic lifestyle, such as protein denaturation and membrane fusion, a number of mechanisms have arisen to provide desiccation tolerance in the seeds of higher plants (for a review, see Macherel et al., 2007). An example of such an adaptation is the accumulation of members of a diverse group of proteins, known as late embryogenesis abundant (LEA) proteins, during the final stages of seed desiccation (Galau et al., 1986). The identification and characterisation of an LEA protein localised in the matrix space of mitochondria (LEAM) in pea (Pisum sativum) led to the findings that during desiccation, LEAM undergoes a conformational change that facilitates its insertion into the inner membrane, conferring desiccation protection to this vital site of cellular energy metabolism (Grelet et al., 2005; Tolleter et al., 2010). This could be one of the essential steps in the degeneration of mature mitochondria into promitochondrial structures; however, an intensive examination of mitochondria during embryogenesis and seed maturation is required to validate this hypothesis. As mitochondria cannot arise de novo, the promitochondrial structure must have all the components necessary to facilitate differentiation into a fully functional mature mitochondrion. Thus, despite their differences in morphology, promitochondria must contain the mitochondrial genome and the cognate machinery required to express this genome, despite much of this machinery being synthesised in the cytosol and imported along with some species of tRNAs. The import of these mitochondrial proteins requires energy, in the form of both ATP and a membrane potential, so promitochondrial structures must be capable of supporting both. In terms of a membrane potential, it should be noted that as little as 30 mV is sufficient to support protein import, compared to the several-fold higher levels that drive ATP production via oxidative phosphorylation (Pfanner and Neupert, 1985). Additionally, it has been shown in plant mitochondria that oxidation of external NADH (which have been demonstrated to be active in imbibed seeds) by alternative oxidase (AOX) is capable of supporting protein import, as this results in the generation of a sufficient membrane potential (Whelan et al., 1995). In terms of ATP, almost immediately upon imbibition, low levels of oxygen consumption and substrate level phosphorylation are likely to be sufficient to support import. In fact, the amount of ATP required for protein import into mitochondria is likely small in comparison to that required for protein synthesis (Piques et al., 2009). Thus, while promitochondrial structures differ to mitochondria with high metabolic activities seen in various organs or tissues, they cannot be viewed as being devoid of any metabolic activity. Rather, it appears that the proteins required for this activity are present in dry seeds and upon imbibition are activated to prime mitochondrial biogenesis (Ehrenshaft and Brambl, 1990; Howell et al., 2006; Logan et al., 2001). Likewise, mature mitochondria, which display high levels of metabolic activity, still retain a biogenesis capacity. Thus, promitochondria and mitochondria represent an organelle where both biogenesis and

Please cite this article as: Law, S.R., et al., Mitochondrial biogenesis in plants during seed germination, Mitochondrion (2014), http://dx.doi.org/ 10.1016/j.mito.2014.04.002

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metabolic functions are present but are differentiated by the relative amount of each of these activities. It is worth investigating the potential presence of promitochondrial structures in many cell types, which might have previously been ignored; due to a combination of low abundance and confusion with mitochondria damaged during sample preparation. Correspondingly, it should not be ruled out that reduced populations of mature mitochondria may persist in the dry seed, prior to imbibition. 2.3. Transcriptomic analysis of mitochondrial biogenesis during seed germination In maize, northern blot analysis revealed that transcripts encoding proteins associated with mitochondrial bioenergetics (such as atpa, atp9, coxI, coxII and coxIII), exhibited low abundance throughout the early time points, followed by significant increase in abundance between 24 and 48 hours after imbibition (HAI) (Logan et al., 2001). Transcriptomic analysis of genes encoding mitochondrial proteins during rice germination furthered these observations by identifying an early peak in abundance at 3 HAI largely for genes encoding transport functions (Howell et al., 2009). This was followed by a later surge in transcript abundance at 12 HAI, for an over-representation of transcripts encoding proteins associated with mitochondrial energy and metabolism functions (Howell et al., 2009). Importantly, the suite of transcripts up-regulated at 3 HAI were specifically enriched in mitochondrial functions (and no other energy organelle), suggesting that mitochondrial biogenesis plays a crucial role from the very early stages of seed germination (Howell et al., 2009). These observations are consistent with previous studies in various species, which have observed that oxygen consumption increases rapidly following seed imbibition, through the reactivation of oxidative phosphorylation within mitochondria (Botha et al., 1992; Ehrenshaft and Brambl, 1990). An in-depth transcriptomic study of seed germination in the dicot model plant, Arabidopsis thaliana (Arabidopsis) analysed a time course encompassing freshly harvested seed (H), dry seed following 15 days of dry, dark desiccation (0 h), seed collected at three time points during cold, dark stratification (S) and five time points up to 48 h following the transfer into continuous light post-stratification (SL) (Narsai et al., 2011). An interesting group of genes were identified as showing a unique pattern characterised by a transient peak in expression in the early hours after the transfer from stratification to continuous light (48 h S–6 h SL). An analysis of this group of genes with the AtGenExpress developmental data set (Schmid et al., 2005) revealed that 775 showed a germinationspecific expression, while gene ontology categorisation revealed that approximately double the expected percentage of genes in this set encoded proteins targeted to the mitochondrion (Narsai et al., 2011). Based on this study, further analysis of genes encoding mitochondrial proteins was carried out and a model describing a triphasic progression of transcriptomic events during seed germination was proposed (Law et al., 2012). Firstly, the transient expression of two groups of genes encoding nucleic acid metabolism and protein import and synthesis functions were identified, followed by the progressive increase in transcript abundance of a third group of genes encoding electron transport chain components (Fig. 1). The first group attains maximal transcript abundance at the end of stratification, before the transfer into continuous light and is composed of transcripts encoding proteins with DNA/RNA metabolism functions. These included notably DNA replication, transcription, transcriptional regulation and RNA editing/splicing, specifically there was a significant overrepresentation of mitochondrial targeted pentatricopeptide repeat proteins (PPRs) in this group (Fig. 1A). PPRs are predominately mitochondrial or plastid targeted proteins that have been demonstrated to have a diverse array of RNA metabolism functions, including: transcription (Ding et al., 2006), RNA editing (ChateignerBoutin et al., 2008), splicing (de Longevialle et al., 2008), processing (Nakamura et al., 2003), stability (Yamazaki et al., 2004) and translation (Choquet and Wollman, 2002). Interestingly, PPR encoding genes in rice

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do not show the transient expression pattern that is seen in Arabidopsis (Narsai et al., 2011). Instead, PPR proteins in rice are enriched in the group of transcripts showing the highest expression in the dry seed and then decreasing to a much lower level over the course of germination (Howell et al., 2009). While there appears to be a conserved requirement for the highest expression of these regulatory components during the early hours of germination, the transient nature of this expression, as seen in Arabidopsis (Law et al., 2012; Narsai et al., 2011) may not necessarily be a conserved pattern of expression for these in all plants. A more extensive time course analysis of rice germination could reveal where these differences are biological or the result of experimental design. It was also observed that the transient burst in expression of genes encoding these mitochondrial functions occurs coincident with a peak in expression of transcripts encoding proteins associated with cytosolic nucleotide metabolism and the factors responsible for conveying these nucleotides into the matrix. These observations suggest the coordinated accumulation of nucleotides so they can be utilised for the transcription of mitochondrially encoded proteins. Proteins associated with DNA and RNA metabolism have been previously demonstrated to display rapid rates of protein turnover, with proteins belonging to this category displaying some of the highest average synthesis and degradation rates (KS and KD, respectively) of any functional category, in whole extracts of Arabidopsis cell culture (Li et al., 2012). A subsequent study examining degradation rates for mitochondrial proteins made consistent observations, with many enzymes involved in mitochondrial DNA and RNA processes turning over rapidly, with one member, glycine-rich RNA binding protein 2 (GR-RBP2), exhibiting the sixth fastest turnover rate of any mitochondrial protein (Nelson et al., 2013). A corresponding study which examined global mRNA decay rates in Arabidopsis also observed that degradation rates of transcripts encoding proteins with RNA metabolism functions (specifically transcription factors and PPR proteins) have some of the shortest half-lives of any transcript species observed (Narsai et al., 2007). These observations highlight the importance of the transient nature of this initial burst in the expression of DNA and RNA metabolism functions, particularly for the rapid and coordinated degradation of these transcripts (and possibly the encoded proteins) in the early hours of exposure to light, following stratification. This is supported by previous findings, which have shown that perturbation to mRNA decay during seed germination often has major deleterious effects on the normal development of the germinating seed (Delseny et al., 1977; Nishimura et al., 2005; Yoine et al., 2006). Taken together, these findings suggest that proteins with DNA and RNA metabolism functions are not simply acting to maintain mitochondria through the constitutive management of the mitochondrial transcript pool but rather by providing a decisive and fleeting function in establishing mitochondria at the outset of seed germination. The second group of genes is expressed very shortly after and is composed of transcripts encoding protein metabolism functions, such as ribosomes, translation factors and tRNA-related functions (Fig. 1B). Comparative analysis of this transcript data with corresponding protein abundance data (carried out using mass spectrometry) revealed strong levels of concordance between these during germination, confirming that this rapid induction and degradation of transcripts with protein metabolism functions is observed at both the protein and transcript level (Narsai et al., 2011). In addition, the transcript abundance of proteins associated with mitochondrial protein import, such as components of the TOM and TIM complexes, are also reaching maximal abundance levels, suggesting that the import of nuclear-encoded mitochondrial proteins may occur simultaneously with the synthesis of organelle-encoded proteins. This coordination is not surprising, as many mitochondrial protein complexes are made up of both nuclear and organelle encoded subunits, and successful assembly necessitates careful control over subunit accumulation and stoichiometry (Jansch et al., 1996). The expression of these biogenesis factors early in the

Please cite this article as: Law, S.R., et al., Mitochondrial biogenesis in plants during seed germination, Mitochondrion (2014), http://dx.doi.org/ 10.1016/j.mito.2014.04.002

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Fig. 1. Transcript profiling of mitochondrial proteins reveals the progressive phases of mitochondrial biogenesis (adapted from Law et al., 2012). Seeds were collected at ten time points, including H (freshly harvested); 0 h (dry seed following 2 weeks of dessication); three time points during stratification (S), 1 h S, 12 h S and 48 h S; and 5 time points during continuous light following stratification (SL), 1 h SL, 6 h SL, 12 h SL, 24 h SL and 48 h SL. The abundance of transcripts encoding mitochondrial proteins was normalised to the maximal expression of each transcript and separated into three groups based on their encoded protein function. (A) Transcripts encoding proteins associated with DNA and RNA metabolism. (B) Transcripts encoding proteins associated with protein synthesis and import. (C) Transcripts encoding proteins associated with the electron transport chain. Both (A) and (B) displayed transient expression, with the transcripts of group (A) peaking between 48 h S and 1 h SL (I), and transcripts of (B) peaking between 1 h SL and 6 h SL (II). Transcripts in group (C) were observed to accumulate as the time course progressed, with maximal expression observed between 24 h SL and 48 h SL (III). (For interpretation of the references to colour in this figure, the reader is referred to the web version of this article.)

germination time course further emphasises the crucial role of mitochondrial biogenesis for successful seed germination (Law et al., 2012). Similar to the observations made in maize and rice, the third group of mitochondrial transcripts encodes proteins involved in bioenergetics such as components of the ETC, which were observed to increase in abundance as seed germination progressed before reaching maximum levels at the end of the time course (Howell et al., 2009; Logan et al., 2001) (Fig. 1C). This phase represents the final steps in the transition of the promitochondria to mature mitochondria, as characterised by a greatly reduced emphasis on biogenesis, and accompanied by an

increase in bioenergetic and metabolic functionality as required during the vegetative stages of plant development. 3. Evolutionary age of mitochondrial genes during seed germination A study that investigated the evolutionary age of genes expressed during seed germination revealed a ‘germinative hourglass,’ characterised by maximal expression of evolutionarily young genes at the beginning (shortly after imbibition) and end of seed germination (following radicle protrusion), punctuated by a period of minimal expression during the

Please cite this article as: Law, S.R., et al., Mitochondrial biogenesis in plants during seed germination, Mitochondrion (2014), http://dx.doi.org/ 10.1016/j.mito.2014.04.002

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midpoint of seed germination (Dekkers et al., 2013). Evolutionarily ancient genes exhibited an inverse expression pattern, with low transcript abundance at the beginning of germination, followed by a transient peak in abundance at testa rupture and then decreasing to low levels by the end of the time course (radicle emergence) (Dekkers et al., 2013). These observations mirror those made in a previous study that examined the evolutionary age of genes expressed during embryogenesis in Arabidopsis (from zygote to mature seed) (Quint et al., 2012). To investigate the effect of the evolutionary age on mitochondrial transcripts, the list of 1035 genes encoding mitochondrial proteins, as defined by Law et al. (2012), was cross-referenced with the phylostratigraphic (PS) ranking established by Quint et al. (2012). In this way, the rank of each gene found to be displaying maximal expression at a given time point was averaged and recorded. As a point of reference, this was also carried out for the whole genome set (Fig. 2). Interestingly, though the whole genome set displayed an analogous transcriptome profile to that presented by Dekkers et al. (2013), the mitochondrial list was observed to display the opposite of this, with evolutionarily old genes expressed both at the beginning and end of Arabidopsis germination, interrupted by the transient expression of younger genes at 48 h SL and 1 h SL (Fig. 2). Closer inspection of the mitochondrial genes expressed during these time points reveals the source of this abundance of evolutionarily young genes. Of the hundreds of genes expressed transiently in the mitochondrial set, including transcription factors, tRNA-related functions, ribosomes and protein import components (n = 167; average PS = 1.6), only members of the PPR family are consistently classed in the phylostratigraphically young (PS 4, 5, 6 and 7) gene groups and the shear abundance of transiently expressed mitochondrial PPRs (n = 149; average PS 4.4) influences the entire mitochondrial set. Thus, the high number of PPRs expressed at this point during seed germination likely illustrates the relatively recent evolution of some of the major regulatory mechanisms underpinning mitochondrial biogenesis in plants. Additionally, this is particularly interesting as the number of PPR encoding genes is much larger in plants than mammalian species, supporting a unique, and apparently more recent divergence of this family in the evolution of land plants (Lurin et al., 2004). 4. The mitochondrion as a signalling hub during seed germination The mechanical story of mitochondrial biogenesis during seed germination is becoming increasingly well established, with a number of studies describing the stepwise maturation of promitochondria into

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metabolically active mitochondria, which have a central role in the cellular landscape as a source of ATP (Howell et al., 2006; Law et al., 2012; Logan et al., 2001). In addition, the literature regarding plant responses to biotic and abiotic stresses has long recognised the mitochondrion as a focal point for stress perception and signalling (Schwarzlander et al., 2012; Van Aken et al., 2009; Vanlerberghe, 2013). For sessile organisms such as plants, the ability to respond efficiently to biotic and abiotic stresses is critical to plant growth and productivity. Thus, it is useful to view the mitochondrion as more than just a source of cellular energy, but also as a signalling hub, capable of perceiving and consolidating numerous signals originating in the nucleus (known as anterograde signalling) and transmitting signals of their own back to the nucleus, in order to regulate responses based on perceived stresses or developmental checkpoints (known as retrograde signalling) (Leister, 2012). The majority of the regulatory traffic between the nucleus and the energy organelles is anterograde in nature. An example of anterograde regulation is the recruitment of specific transcription factors to cis-acting regulatory elements (CAREs), within the promoters of nuclear encoded organelle genes, to regulate diverse processes such as cell proliferation, organ identity and nutrient perception (Girin et al., 2007; Luo et al., 1999; Nath et al., 2003). In contrast, retrograde signals are often associated with coordinating complex stress responses. For example, a study by Rizhsky et al. (2004) in Arabidopsis observed a highly conserved transcriptomic response to cold, drought and high salinity conditions, but a dissimilar response between drought and heat conditions. Through the consolidation of these anterograde and retrograde signals, mitochondria play a central role in coordinating the metabolic and signalling homeostasis of the cell and, thus, optimise plant viability during stress. These signals are also pivotal to the assembly of the numerous nuclear and organelle encoded subunits that make up each complex of the respiratory chain, which requires a tremendous level of coordination. Additionally, it has been suggested that these avenues of communication facilitate the monitoring of mitochondrial abundance, to ensure the correct distribution of mitochondrial numbers during cellular division (Battersby and Richter, 2013). It has been previously demonstrated that disruption to mitochondrial function can impair cell proliferation, an observation that was commonly attributed to a reduction in the energy pool as a consequence of dysfunction to mitochondrial respiration (Escobar-Alvarez et al., 2010; Van Aken et al., 2007). However, a recent study in mouse embryonic fibroblasts (MEFs) has demonstrated that cellular proliferation is arrested by the stalling of mitochondrial ribosomes and that the observed reduction in metabolic potential is purely a downstream

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Time point Fig. 2. Investigation of the evolutionary age of genes during seed germination. Seeds were collected at ten time points, including H (freshly harvested); 0 h (dry seed following 2 weeks of dessication); three time points during stratification (S), 1 h S, 12 h S and 48 h S; and 5 time points during continuous light following stratification (SL), 1 h SL, 6 h SL, 12 h SL, 24 h SL and 48 h SL. A list of 1035 genes defined as encoding mitochondrial proteins (defined in Law et al., 2012) was cross-referenced with the phylostratigraphic ranking established in Quint et al. (2012), and the rank of each gene found to be displaying maximal expression at a given time point (data from Narsai et al., 2011) was averaged and plotted. This was also carried out for the whole genome set and the mitochondrial list minus PPR proteins. (For interpretation of the references to colour in this figure, the reader is referred to the web version of this article.)

Please cite this article as: Law, S.R., et al., Mitochondrial biogenesis in plants during seed germination, Mitochondrion (2014), http://dx.doi.org/ 10.1016/j.mito.2014.04.002

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the role of mitochondria in the regulation of cellular proliferation during seed germination.

consequence of this dysfunction (Richter et al., 2013). According to the authors, this stalling activates a pathway to rescue dysfunctional ribosomes, which in turn elicits the degradation of mitochondrial rRNA and mRNA pools and arrests cell proliferation via a retrograde signal (Richter et al., 2013). Additionally, translational stress has also been advanced as an initiator of retrograde signals in plants. It has been shown that null mutants of the PROLY-tRNA SYNTHETASE1 (PRORS1) protein, which is targeted to both the mitochondria and chloroplasts, result in the arrest of embryo development (Pesaresi et al., 2006). However, mutants with leaky alleles of PRORS1, exhibited a down-regulated expression of nuclear encoded genes associated with photosynthetic light reactions. This down-regulation was independent of light or photooxidative stress, suggesting that the observed down-regulation of photosynthetic machinery occurred by means of retrograde signals originating from the mitochondria and chloroplast, as a consequence of translational stress (Pesaresi et al., 2006). In light of this, the transient expression of mitochondrial translational machinery during early seed germination in Arabidopsis (Law et al., 2012) represents a potentially crucial checkpoint for the monitoring of mitochondrial homeostasis and emphasises

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The endosymbiotic event that gave rise to the mitochondrion has established a complex relationship between the organelle and its cellular environment. While mitochondria display large differences between phylogenetic groups, they also display many similarities that reveal their common origin. However, even in a single organism, mitochondrial populations display heterogeneity in terms of morphology, protein content and activity between different tissues and developmental processes (Lee et al., 2008, 2012; Peters et al., 2012). The promitochondrial structures observed in dry seeds represent one extreme of this variation and, during seed germination, exhibit the transient expression of many components involved in biogenesis (DNA/RNA and protein metabolism) to an extent not observed in any other vegetative plant tissue or development stage and yet retains some metabolic activity (Fig. 3). Thus, seed germination offers unique opportunities to study mitochondrial

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Fig. 3. A model for mitochondrial biogenesis during seed germination (adapted from Law et al., 2012). Seeds were collected at ten time points, including H (freshly harvested); 0 h (dry seed following 2 weeks of dessication); three time points during stratification (S), 1 h S, 12 h S and 48 h S; and 5 time points during continuous light following stratification (SL), 1 h SL, 6 h SL, 12 h SL, 24 h SL and 48 h SL. Promitochondrial structures in dry seeds lack cristae and the protein complement associated with mature mitochondria. The transient expression of transcripts encoding proteins with RNA and DNA metabolism functions and nucleotide synthesis and import occurs at the transition of the seed from stratification into continuous light. This is followed shortly by the transient expression of transcripts encoding proteins with protein metabolism and import functions. The nest stage that occurs after 24 h of transfer to light is the increase in transcript abundance of genes encoding various metabolic components, primarily those associated with the TCA cycle and the electron transport chain. This procession of events is regulated through the coordinated communication between the nucleus and the mitochondrion; known as anterograde and retrograde regulation. (For interpretation of the references to colour in this figure, the reader is referred to the web version of this article.)

Please cite this article as: Law, S.R., et al., Mitochondrial biogenesis in plants during seed germination, Mitochondrion (2014), http://dx.doi.org/ 10.1016/j.mito.2014.04.002

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biogenesis under a degree of synchrony. However, the technical barriers of working with dry seeds need to be overcome, through the adoption of a combination of cell-specific approaches and in vivo approaches that facilitate observation to the level of an individual mitochondrion or small groups of mitochondria. While challenging, these approaches have the potential to reveal specific regulatory and signalling aspects of mitochondria that may be more elusive in cells where mitochondrial function is more established, and thus are worth pursuing.

Acknowledgements This work was supported by grants to J. W. from the Australian Research Council (CEO561495 and CE140100008).

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