Review
Endosymbiosis and evolution of the plant cell

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Abstract

The bacterial origins of plastid division and protein import by plastids are beginning to emerge — thanks largely to the availability of a total genome sequence for a cyanobacterium. Despite existing for hundreds of millions of years within the plant cell host, the chloroplast endosymbiont retains clear hallmarks of its bacterial ancestry. Plastid division relies on proteins that are also responsible for bacterial division, although may of the genes for these proteins have been confiscated by the host. Plastid protein import on the other hand relies on proteins that seem to have functioned originally as exporters but that have now been persuaded to operate in the reverse direction to traffic proteins from the host cell into the endosymbiont.

Introduction

‘Picture a palm tree growing peacefully on the shore of a spring, and a lion, lying hidden beside the palm, all its muscles tense, blood lust in its eyes, ready to pounce on an antelope and slaughter it. In order to understand fully the inner secret of this picture with its two such drastically different manifestations of life, a palm tree and a lion, it is essential to appreciate the theory of endosymbiosis. The life of the palm tree is so calm and peaceful because it is a symbiosis, it contains a legion of workers, green slaves (plastids) that work for it and nourish it. The lion has to feed itself.

Imagine that every cell of the lion’s body was filled with plastids, and I have no doubt that it would immediately lay itself peacefully by the palm, feeling replete with nothing more than some water and a few nutrient salts.’

Mereschkowsky, 1905 [1]

The acquisition of plastids by eukaryotic cells must rank as one of the most momentous events in the planet’s history; for plant cells it was their defining moment. Schimper [2] seems to have been the first biologist to realise that plastids derive from endosymbiotic photosynthetic bacteria (Figure 1), but it was Mereschkowsky [1] who elaborated the concept in eloquent detail. Modern research is painting in more and more detail Mereschkowsky’s idyllic picture of a bacterial cell living within a nucleated host cell. The availability of whole cyanobacterial genome sequences, combined with the advantage of being able to extrapolate from bacterial systems, which can be used to model events in chloroplasts, has allowed us to probe many of the questions of chloroplast biology with unprecedented finesse. My review focuses on the recent rapid progress in our understanding of how the endosymbiont divides and how its need for host-encoded proteins is satisfied.

Section snippets

Chloroplast division

To establish a permanent endosymbiosis (i.e. one not requiring ongoing recruitment of fresh endosymbionts) the endosymbiont must divide within the host cells. Daughter endosymbionts must then be segregated into each daughter host. Little is known about these processes at the molecular level [3]. Most plant cells contain numerous chloroplasts (or plastids) that divide throughout the plant cell cycle (Figure 1), which perhaps suggests that the segregation process is only loosely regulated.

Intracellular gene transfer and transit peptides

A free-living cyanobacterium possesses about 3,000 genes [16] but a chloroplast has only 100–200 genes [17••]. Clearly, numerous genes such as those coding for peptidoglycan wall synthesis, became dispensable when the bacterium took up residence within the confines of a host, and these were probably lost; it is also clear that many indispensable genes have relocated to the plant cell nucleus [17••]. Estimates of 1000–5000 nuclear genes encoding chloroplast proteins have been postulated 17••,

Chloroplast protein import machinery

Intra-chloroplast protein targeting has long been known to derive from the endosymbiont secretion machinery [39] and several recent papers confirm this origin 40, 41, 42, 43, 44. For many years the ΔpH-dependent pathway involved in thylakoid protein targeting was thought to be an exception to this rule and was regarded as a specific invention of chloroplasts. It is now becoming clear, however, that chloroplast hcf106 (high chlorophyll fluorescence) — a protein central to ΔpH-dependent targeting

Plastid targeting in unicellular ‘plants’

The plastids of many protists groups are bounded by multiple membranes, which present additional obstacles for protein targeting. As in plant chloroplasts, targeting is mediated by N-terminal extensions but in these organisms a bipartite, or even tripartite, N-terminus is evident 59, 60•. The first portion of the leader, which is nearest to the N-terminus, comprises a classic, hydrophobic signal peptide for secretion into the endomembrane system 61•, 62•. The second component is a hydrophilic

Conclusions

Chloroplasts arose from cyanobacterial-like endosymbionts that were engulfed by a eukaryotic heterotroph about 1 billion years ago. The availability of the complete genome sequence for a cyanobacterium now allows us to frame hypotheses for the mechanisms of chloroplast division and the targeting of nuclear-encoded proteins into the organelle. Although much of the original endosymbiont machinery appears to be conserved, some components have undergone substantial modification to either change or

Acknowledgements

I thank the Australian Research Council for support and Sue Barnes for Figure 1b. Errors in the translation of Mereschkowsky [1] are mine.

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

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