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| This article will appear in a forthcoming issue of Trends in Plant Science. | |
Editor's Note:
Joachim Messing in his recent "Comment" [1] discussed the remarkable similarity in gene count between the human [2,3] and Arabidopsis thaliana genomes [4]. No one knows why the number of open-reading-frames (ORFs) in the Arabidopsis genome (25,500) [4] is only slightly less than that estimated for the human genome (31,500) [2,3] - specifically, how humans can get by with so few genes - but we can answer Messing's opening question "Do plants have more genes than humans?" in the affirmative in at least some cases. The ATP-binding cassette (ABC) proteins are a case in point, many of which are modularly constructed membrane proteins containing idiotypic nucleotide-binding folds (NBFs). By compiling the first complete inventory of the ABC protein superfamily from Arabidopsis [5] - the first complete inventory of ABC proteins from any multicellular organism - we have determined that the genome of this plant encodes 129 ABC proteins, which fall into 13 subfamilies (figure 1). This gene count far outstrips those for the human genome and for any other animal genome sequenced to date. The human genome is estimated to encode a mere 51 ABC proteins; those of Caenorhabditis elegans (19,000 ORFs) and Drosophila melanogaster (13,600 ORFs) only 58 and 55, respectively.
The results from Arabidopsis are equally impressive when viewed in another way - through the transport physiologist's eye. Of the total ABC protein ORFs identified in Arabidopsis, ∼103 probably encode membrane transporters - proteins possessing membrane spans contiguous with one or two NBFs (reference 5 and ArabidopsisABC.net) Taking this into account, when the rough equivalence of the total transporter gene complement of Arabidopsis (700 ORFs) is compared with those of animals such as C. elegans (650 ORFs) and Drosophila (600 ORFs) [4], it is evident that Arabidopsis allocates nearly twice as many of its transporter genes to ABC transporters as do C. elegans or Drosophila.
The forces, evolutionary or otherwise, responsible for the disproportionate allocation of coding sequences to ABC proteins - and of the total transporter gene complement to ABC transporters - in Arabidopsis, and presumably other plants, can only be speculated. However, given the inherently greater capacity of transporters, such as ABC transporters, which are directly energized by ATP, versus H+-coupled secondary transporters, for establishing steep concentration gradients across membranes under the conditions that prevail in vivo [6] and the fact that most characterized eukaryotic ABC transporters (albeit a small fraction of those that are now known to exist) have been implicated in the transport of secondary metabolites, organic xenobiotics, and other complex amphiphiles [6,7], several factors come to mind. Most notable of these is the extraordinary metabolic versatility of plants. More than 100,000 secondary metabolites have been identified in plants [4], most of which would be toxic to the cells that produce them, even at pharmacological concentrations, if they were not transported across membranes out of the compartments in which they are synthesized against steep concentration gradients [6,7]. Furthermore, although the capacity of green plants for photosynthesis greatly augments their metabolic versatility, this process and its photo-oxidative consequences, places even greater demands on the cellular detoxification machinery. As if this were not enough to contend with, plants not only manufacture their own secondary products but also have to suffer those of other organisms, for example allelochemicals and microbial metabolites and chemicals associated with humans and their various environmentally destructive activities. In combination, all these factors, plus the sessile lifestyle of plants - their inability to exercise speedy avoidance behaviors - and their frequent lack of specialized excretory structures, necessitate cellular detoxification mechanisms of exquisite range and sophistication.
It is probably no coincidence that members of another gene superfamily implicated in secondary metabolism and xenobiotic detoxification, the cytochromes P450, are also disproportionately represented in plants compared with animals. The Arabidopsis genome encodes 286 putative cytochromes P450 [4], three- to fourfold more than the numbers predicted from the genome sequences of C. elegans (73 ORFs) and Drosophila (94 ORFs).
Gene and protein head counts are not an end in themselves but instead constitute component toolboxes for meaningful functional analyses and intraorganismal and interorganismal comparisons. This is especially true of the Arabidopsis ABC protein superfamily. The amenability of Arabidopsis to transcriptomic, proteomic, and reverse genetic approaches, combined with its possession of such an extended and hierarchical family of ABC proteins, will probably lead to completely new insights into the mechanistic basis of a wide range of processes.
