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The Plant Cell 19:1135-1138 (2007) © 2007 American Society of Plant Biologists
Thylakoid Development from Biogenesis to Senescence, and Ruminations on RegulationNews and Reviews Editor neckardt{at}aspb.org
Anyone who has watched trees and other plants leafing out in the spring in temperate regions is aware that chloroplast development can occur rapidly in the light. The grass in lawns seems to turn green in a single morning. And yet chloroplasts, and thylakoids, the membrane-bound compartments inside them where the light-dependent reactions of photosynthesis take place, are highly complex both structurally and functionally. Thylakoid membranes contain the chlorophylls and hundreds of integral proteins organized into the light-harvesting antenna complexes (LHCI and LHCII) and the four major complexes that carry out the light reactions of photosynthesis: photosystem I, photosystem II (PSII), the cytochrome b6f complex, and ATP synthase. These complexes contain both nuclear- and plastid-encoded subunits, requiring coordination of gene expression in these compartments and efficient translocation of nuclear-encoded factors into the chloroplast.
Not surprisingly, there are many mutations affecting these complexes that may show deficiencies in thylakoid development and characteristics of reduced chlorophyll content and photosynthesis. However, teasing out the mechanisms that regulate thylakoid development is more difficult. A loss-of-function mutation causing a defect in thylakoid development does not necessarily indicate that the encoded protein regulates thylakoid development. Pichersky (2005)  noted that "the incantatory invocation of [regulation] and similar terms and the reflexive affixation of the adjective ‘regulatory’ to any cellular component whose modification leads to a changed outcome provide us with only the illusion of deeper mechanistic understanding." Owing to the wide range of uses of the terms regulation and control, Pichersky (2005) does not attempt a definition but merely asks that we engage in a public discussion of their meaning and utility in cellular and molecular biology. This issue of The Plant Cell includes four articles that deepen our understanding of thylakoid development and the factors and processes that either control or influence it, from biogenesis through senescence. In addition, a review of these articles may be instructive in the continued discussion of what constitutes regulation.
Etiolated plants grown in darkness typically lack chlorophyll and appear white or pale yellow because thylakoid formation (in angiosperms) requires light. In the absence of light (and in the plant embryo), proplastids develop into etioplasts containing membranous structures called prolamellar bodies, which rapidly develop into thylakoids when exposed to light. Light signals are perceived by photoreceptors, mainly the phytochromes, initiating a complex cascade of interacting signal transduction pathways.
One of the essential components in early thylakoid formation is VESICLE-INDUCING PROTEIN IN PLASTIDS1 (VIPP1). VIPP1 is highly conserved among photosynthetic organisms and is required for thylakoid membrane formation but not for the assembly of the thylakoid membrane protein complexes (Aseeva et al., 2007
Another factor that has been shown to be critical in thylakoid formation and maintenance is the nuclear-encoded membrane-anchored ATP-dependent protease FtsH. Functional FtsH appears to be a complex consisting of multiple FtsH subunits. For example, Arabidopsis has 12 FtsH homologs, nine of which are targeted to chloroplasts (Sakamoto et al., 2003
The work of Miura et al. might help to deepen our understanding of regulation. FtsH exhibits proteolytic activity against a number of thylakoid proteins, and there is evidence for roles in thyakoid maintenance (repair of photodamaged proteins) and in the early stages of thylakoid formation (reviewed in Sakamoto, 2006 ). The extreme phenotype with a predominance of white sectors in leaves of var1 var2 double mutants shows that these FtsH proteases are essential for normal thylakoid formation. However, rather than categorizing FtsH as regulatory, Miura et al. place more emphasis on the balance between the processes of protein synthesis and degradation in chloroplasts exerting control over thylakoid formation. This conclusion was based on the characterization of second-site mutations, such as fug1 and sco1, that suppress the leaf variegation phenotype of var1 and var2 mutants. Whereas the VAR genes encode FtsH proteases associated with thylakoid protein degradation, Miura et al. found that FUG1 encodes chloroplast prokaryotic translation initiation factor2, suggesting that it functions in chloroplast protein synthesis. A loss-of-function mutation of SCO1, which encodes chloroplast elongation factor G (Albrecht et al., 2006), was also found to suppress var1 and var2 phenotypes (see figure
). Additional experiments showed that fug1 and sco1 mutants are deficient in translation of chloroplast proteins, such as D1.
It has been postulated that variegation occurs in the var mutants because a certain threshold level of FtsH proteins is necessary for normal thylakoid development, and loss of FtsH subunits occurs in a cell-autonomous fashion in the mutants (Yu et al., 2004 ; Zaltsman et al., 2005). Miura et al. hypothesize that decreased protein synthesis in chloroplasts due to fug1 and sco1 second-site mutations in a var2 or var1 background would lower the threshold levels of FtsH required for thylakoid formation by restoring the balance between protein synthesis and degradation.
The importance of balance between protein synthesis and degradation for thylakoid formation and maintenance can also be seen from the work reported in three other articles in this issue by Schult et al. (pages 1329–1346), Sun et al. (pages 1347–1361), and Kusaba et al. (pages 1362–1375). It has long been recognized that the PSII reaction center D1 protein has an exceptionally high rate of turnover (Eaglesham and Ellis, 1974 ; Mattoo et al., 1984). Its location and function at the core of the PSII reaction center render it highly susceptible to photodamage, and rapid turnover of the protein is considered essential for avoiding or mitigating photoinhibition under high light (e.g., Aro et al., 1993). Miura et al. did not investigate in detail whether variegation and its suppression in var and fug1 mutants is associated with balancing synthesis and degradation of a particular chloroplast protein. However, they showed that the fug1 mutation led to a decrease in D1 synthesis, and Bailey et al. (2002) previously found that FtsH2 degrades D1 in a light-dependent manner. Silva et al. (2003) and Yoshioka et al. (2006) provided additional evidence that FtsH proteins are involved in the primary cleavage of photodamaged D1. Miura et al. speculate that a balance of synthesis and degradation of D1 protein could be a critical feature of var mutants: the accumulation of photodamaged D1 due to loss of FtsH proteins in var mutants might be a key element in the development of variegated sectors, whereas fug1 might prevent variegation by limiting the accumulation of photodamaged D1.
The work of Sun et al. focuses on degradation of D1 by DEGP protease complexes containing DEG5 and DEG8. DEGP proteases are widely distributed in eukaryotes and are believed to have an important function in degradation of misfolded or aberrant soluble and membrane proteins (Clausen et al., 2002
The authors next identified T-DNA insertion mutants of deg5 and deg8 and generated deg5 deg8 double mutants. Experiments with mutant plants showed that DEG5 and DEG8 are required for efficient PSII repair under high light and protection against photoinhibition in vivo, likely due to a role in D1 protein degradation. Kapri-Pardes et al. (2007) Meanwhile, Schult et al. found that the nuclear-encoded factor HIGH CHLOROPHYLL FLUORESCENCE 173 (HCF173) is essential for PSII biogenesis in developing thylakoids due to an impact on D1 synthesis. HCF173 has weak similarity to short-chain dehydrogenases/reductases, and polysome association experiments showed that it is involved in the inititation of translation of the chloroplast gene psbA, which encodes D1. Mutant hcf173 seedlings have a high chlorophyll fluorescence phenotype and are unable to grow photoautotrophically on soil (but can be maintained on sucrose-supplemented medium). A lack of HCF173 resulted in drastically reduced D1 synthesis, which also led to a failure to accumulate other PSII subunits. This work shows that HCF173 is an essential factor for D1 synthesis. Nonetheless, it is not necessarily helpful or accurate to label the protein as regulatory. The authors acknowledge that they have not determined whether HCF173 is involved in "basic aspects of D1 synthesis or instead is part of the regulatory apparatus adjusting psbA mRNA translation," which again might imply that regulation is more properly associated with balancing or adjusting flux through certain pathways or processes. In relation to the balance hypothesis of Miura et al., it would be interesting to investigate whether decreased synthesis of D1 using partial loss-of-function alleles of hcf173 would suppress the leaf variegation phenotype of var mutants.
On the other end of the spectrum of thylakoid maintenance from biogenesis to senesence, Kusaba et al. found that the inhibition chlorophyll b degradation in non-yellow coloring1 mutants of rice results in a stay-green phenotype, suggesting that chlorophyll b degradation might be an important regulatory point in leaf senescence. The authors show that conversion of chlorophyll b to a is a key step initiating the degradation of chlorophyll b and subsequent degradation of light-harvesting complexes and thylakoids during senescence. The efficient degradation of chlorophylls and thylakoids may be an important aspect of senescence, since intermediates of chlorophyll degradation or free chlorophyll molecules are highly reactive and could be harmful.
It is interesting to note that some cell death mutants, such as acd1 and acd2, which show an enhanced cell death phenotype, are also associated with defects in chlorophyll degradation (Mach et al., 2001 These four articles reveal important characteristics of some of the essential factors involved in thylakoid development. All four contribute to the notion that balancing the processes of synthesis and degradation of various thylakoid components is an important concept in arriving at a deeper understanding of the mechanisms that regulate thylakoid formation throughout plant development. In addition, these works demonstrate that a detailed analysis of any biological process is likely to reveal that there are many components contributing to the final outcome, and changes in any of them may result in a changed outcome. Therefore, it may sometimes be helpful to think of processes (and the attendant balance between or flux through entire pathways), rather than individual components of processes or pathways, as regulatory in terms of the outcome.
www.plantcell.org/cgi/doi/10.1105/tpc.107.052779
Albrecht, V., Ingenfeld, A., and Apel, K. (2006). Characterization of the snowy cotyledon 1 mutant of Arabidopsis thaliana: The impact of chloroplast elongation factor G on chloroplast development and plant vitality. Plant Mol. Biol. 60: 507–518.[CrossRef][ISI][Medline] Aro, E.M., McCaffery, S., and Anderson, J.M. (1993). Photoinhibition and D1 protein degradation in peas acclimated to different growth irradiances. Plant Physiol. 103: 835–843.[Abstract] Aseeva, E., Ossenbühl, F., Sippel, C., Cho, W., Stein, B., Eichacker, L., Meurer, J., Wanner, G., Westhoff, P., Soll, J., and Vothknecht, U. (2007). Vipp1 is required for basic thylakoid membrane formation but not for the assembly of thylakoid protein complexes. Plant Physiol. Biochem. 45: 119–128.[CrossRef][Medline] Bailey, S., Thompson, E., Nixon, P.J., Horton, P., Mullineaux, C.W., Robinson, C., and Mann, N.H. (2002). A critical role for the Var2 FtsH homologue of Arabidopsis thaliana in the photosystem II repair cycle in vivo. J. 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(2006). Quality control of photosystem II. Cleavage of reaction center D1 protein in spinach thylakoids by FtsH protease under moderate heat stress. J. Biol. Chem. 281: 21660–21669. Yu, F., Park, S., and Rodermel, S.R. (2004). The Arabidopsis FtsH metalloprotease gene family: Interchangeability of subunits in chloroplast oligomeric complexes. Plant J. 37: 864–876.[CrossRef][ISI][Medline] Zaltsman, A., Feder, A., and Adam, Z. (2005). Developmental and light effects on the accumulation of FtsH protease in Arabidopsis chloroplasts—Implications for thylakoid formation and photosystem II maintenance. Plant J. 42: 609–617.[CrossRef][ISI][Medline] Related articles in Plant Cell:
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