Introduction

The focus of this chapter is to examine via published data and intuitive reckoning the extent of ER participation in the biogenesis of plant peroxisomes. However, to do this effectively one needs to consider the breadth and variation of peroxisomal biogenesis in all organisms that have been examined. Within this context, we consider biogenesis in the broadest sense that includes all means of: (a) ontogeny/formation of nascent pre-peroxisomes, (b) maturation (elaboration/differentiation) of pre-peroxisomes and preexisting peroxisomes, (c) constitutive duplication of pre-existing peroxisomes during normal cell division, and (d) induced proliferation of pre-existing per-oxisomes independent of normal cell division. These aspects are included with varying emphases within the numerous recent reviews of peroxisome biogenesis in yeasts, mammals, and plants. Thus, rather than giving a comprehensive coverage of original articles, we have decided to cite these reviews.

Figure 1 is a comprehensive integration of the four generalized (main?) peroxisomal biogenesis models, which have been modified for simplicity of presentation. Conspicuous by their absence are the names and locations of specific membrane and matrix proteins (including names of specific perox-ins). Our emphasis is on biogenetic events and trafficking pathways related more to acquisitions of membrane proteins and lipids rather than on the uptake of matrix proteins. In three of the schemes, the ER is shown as the origin of, or significant contributor to, new mature peroxisomes. We have borrowed some key terms from original descriptions and refer to these models in Fig. 1 as follows: the ER-lamellae peroxisome formation pathway (white-black arrows), the ER vesicle-fusion/maturation peroxisome formation/assembly pathway (white arrows), and the ER semi-autonomous peroxisomal growth and division pathway (black arrows). The latter pathway also includes constitutive division and the regulated/induced proliferation of new mature peroxisomes (black arrows). The reader should realize that similar constitutive division and induced proliferation of new mature per-oxisomes should also be shown as extensions of the former two pathways (white-black and white arrows), and are not included for the sake of simplicity. The fourth pathway, referred to as the autonomous peroxisomal growth and division pathway (dashed lines), does not invoke participation of the ER. The source of membrane phospholipids in this pathway (discussed later) is portrayed as an elusive small protoperoxisome.

All four models portray multistep assembly pathways, which enlist a diverse array of membrane and matrix proteins. All of these proteins are synthesized from nuclear-encoded genes because peroxisomes do not possess their own DNA or protein-synthesizing machinery. Accordingly, all of the compartments shown in Fig. 1 acquire their membrane and matrix proteins post-translationally from the cytosol. Matrix proteins are typically imported directly into vesicles, pre-peroxisomes, pre-existing peroxisomes, etc. Details of the cellular and molecular mechanisms for matrix protein import are not described here, but are thoroughly discussed in other reviews (Baker and Sparkes 2005; Erdmann and Schliebs 2005; Mullen 2002). PMPs, including peroxins, enzymes, membrane transporters, etc. may be added from the cytosol directly or indirectly to the various peroxisome compartments. Indirect trafficking typically involves sorting of a subset of so called group I proteins (PMPs) through the ER to peroxisomes (Titorenko and Rachubinski 2001a,b). Group II PMPs bypass the ER and sort directly to peroxisomes. Even in recent reviews and original articles, indirect trafficking of PMPs through the ER has often been labeled controversial. This is based mostly on historical prejudices against ER involvement in peroxi-some biogenesis. This bias is unfortunate because it is misleading; different PMPs may be added directly or indirectly. Interesting and pertinent questions are now whether all PMPs classified as group I or II PMPs in one organism are similarly classified in other organisms, and if not, why have

Fig. 1 multistep peroxisomal assembly models/pathways for different cell types and/or organisms. Each model includes a unique pathway that portrays the biogenesis of new mature peroxisomes. The following are names for each pathway that are used for exploring the involvement of the in ER peroxisomal biogenesis. White-black arrows—ER-lamellae peroxisome formation pathway; White arrows—ER vesicle-fusion/maturation peroxisome formation/assembly pathway; Black arrows—ER semi-autonomous peroxisomal growth and division: constitutive and regulated replication pathway; Dashed lines—Autonomous peroxisomal growth and division pathway. Note that each of the new mature peroxisomes depicted in each pathway are also perceived to undergo constitutive division and/or induced proliferation. This is not shown in all cases for simplicity. Details of individual events and features are described in the text. RER - rough ER

Fig. 1 multistep peroxisomal assembly models/pathways for different cell types and/or organisms. Each model includes a unique pathway that portrays the biogenesis of new mature peroxisomes. The following are names for each pathway that are used for exploring the involvement of the in ER peroxisomal biogenesis. White-black arrows—ER-lamellae peroxisome formation pathway; White arrows—ER vesicle-fusion/maturation peroxisome formation/assembly pathway; Black arrows—ER semi-autonomous peroxisomal growth and division: constitutive and regulated replication pathway; Dashed lines—Autonomous peroxisomal growth and division pathway. Note that each of the new mature peroxisomes depicted in each pathway are also perceived to undergo constitutive division and/or induced proliferation. This is not shown in all cases for simplicity. Details of individual events and features are described in the text. RER - rough ER

these differences evolved? Specific examples of group I and II plant PMPs are considered later.

A family of specialized proteins called peroxins are involved by definition in the various aspects of peroxisomal biogenesis. PEX genes were identified mostly in mutant studies with yeasts. The different peroxins are denoted as PexNp, which is preceded by two letters referring to their genus/species and are numbered consecutively in accordance with recommendations of a special committee (Distel et al. 1996), e.g. AtPex16p denotes Arabidopsis thaliana peroxin 16 protein. Approximately 23 PEX genes (17 kinds of peroxin homologs) have been identified in plants (mostly in Arabidopsis), whereas approximately 17 PEX genes (14 kinds of peroxin homologs) have been identified in mammals, and 34 in yeasts. Since Charlton and Lopez-Huertas (2002) describe them in detail, we do not attempt here to include descriptions of plant peroxin functions as ascribed to each aspect of peroxisomal biogenesis. Also, as mentioned above, Fig. 1 does not show any of the individual sites of peroxin uptake, or any other protein, within these multistep pathways. Protein import varies among the different model organisms, although certain important consistencies are known, especially relative to so-called early peroxins involved in the early stages of peroxisome origination/formation. In these cases, specific peroxins are described later in this chapter.

A knowledge and understanding of the participation of the ER in peroxisomal biogenesis in non-plant organisms is clearly a prerequisite for this chapter. Relatively few model organisms and systems have been studied extensively. These are mammals (mostly human culture cells) (Purdue and Lazarow 2001), yeasts (five different cellular species) (Veenhuis et al. 2000), trypanosomes (mostly Trypanosomal brucei) (Parsons et al. 2001), and the nematode Caenorhabditis elegans (Thieringer et al. 2003). However, little data and consequently few working models on peroxisomal biogenesis specifically focus on plant ER. Work on plants has been mostly with roots and leaves (cotyledons) of common (crop) species and suspension-cultured cells, namely tobacco BY-2 and Arabidopsis cells (Baker and Graham 2002).

A by-product of this low diversity in study systems is that research groups have generally focused on a particular species, or several species within a common group of organisms. Unfortunately, published work on plant cell organelles has not generally been included in discussions of data obtained on non-plant organisms. An undesirable consequence is that interpretations are often incorporated into biogenesis models touted as universally applicable to all organisms regardless of obvious important differences between mammals, yeasts, and plants. Such generalizations are not always correct and it is important and prudent to point out notable exceptions to the models presented by Titorenko and Rachubinski (2001a,b), Mullen et al. (2001a), van der Klei and Veenhuis (2002), Eckert and Erdmann (2003), and Koch et al. (2004). Hence, it is a challenge to identify and segregate those species-specific features from those that are generally applicable.

The assemblage of four generalized models for peroxisomal biogenesis in one comprehensive figure (Fig. 1) is a result of sorting and sifting of published models. This figure is not universally applicable, nor is it intended to represent four mutually exclusive scenarios within one cell or necessarily within different cells in any one organism. Nevertheless, one can identify main sources for each pathway in the figure. The descriptive title coined for each model/pathway (listed above and in the legend of Fig. 1) are intended to focus on the proposed events and actions, rather than on the model or-ganism(s). At this stage, we do not know whether a certain model applies specifically or solely to one organism or species, even though such implications exist in the literature.

The ER-lamellae pathway comes from ultrastructural electron tomo-graphic analyses of mouse dendritic cells (Geuze et al. 2003; Tabak et al. 2003). The ER vesicle-fusion/maturation pathway is derived from a combination of ER-derived vesicle fusion data obtained with the yeast Yarrowia lipolyt-ica (Titorenko and Rachubinski 2001a,b) and vesicle maturation described in Saccharomyces cerevisiae (Hoepfner et al. 2005; Kragt et al. 2005; Kunau 2005; Tam et al. 2005). The ER semi-autonomous growth and division of pre-peroxisomes is based largely on data for plant peroxisomes (e.g., Mullen et al. 1999, 2001a; Trelease 2002; Lisenbee et al. 2003; Karnik and Trelease 2006). The latter pathway partially overlaps with the autonomous growth and division pathway championed by Lazarow (Purdue and Lazarow 2001; Lazarow 2003), and is supported by results obtained by Gould's group (Sacksteder and Gould 2000; South et al. 2000) on mammalian cultured cells and S. cerevisiae.

A key difference between the semi-autonomous and autonomous models is the source of membrane proteins and phospholipids for pre-existing per-oxisomes. In the semi-autonomous scheme, ER-derived vesicles deliver PMPs and phospholipids to growing pre-peroxisomes, whereas in the autonomous scheme membrane remnants or protoperoxisomes, which purportedly are not derived from ER, are envisioned to provide the necessary molecules for self-replicating (autonomous) peroxisomes. Both schemes invoke constitutive formation of daughter peroxisomes prior to, or during, cell division. The portrayal of regulated proliferation comes mostly from numerous contributions with mammalian cells (e.g., Koch et al. 2004) and yeast cells, mostly with Hansenula polymorpha (e.g., Veenhuis et al. 2000). Examples of regulated proliferations are reported for plants in diverse publications briefly discussed and cited below.

In the next sections, we outline and discuss the data, interpretations, and opinions related to the generalized working models presented in Fig. 1. Whenever appropriate, we take the opportunity to insert pertinent information related to plants, and to the plant ER. Models describing peroxiso-mal biogenesis in mammalian cells are considered first for several reasons: (a) because of their historical influence, (b) due to the wealth of pertinent publications, (c) since the adamant conclusions that the ER does not partic ipate in autonomous peroxisomal biogenesis is longstanding, and (d) due to new evidence obtained on mouse (and S. cerevisiae) cells that challenges and refutes anti-ER concepts and conclusions.

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