The fall of Rafflesiales

I have to make a confession - I probably won't be covering a huge number of plants (in the sense of embryophytes) on this blog. This is, I admit, a pretty huge omission. After all, plants are a pretty significant chunk of phylospace, and pretty damn influential in shaping our environment. But compared to animals, plants are scary and complicated and I just don't know all that much about them. That said, I thought I should rectify my previous deficiencies by giving some plants the time of day. I'm not going to completely break with precedent, though - I'm looking at another group of parasites, the "Rafflesiales".

Until very recently, Rafflesiales was an order of holoparasites (i.e. they derive all their nutrition from their host, as opposed to hemiparasites such as mistletoes that still have leaves and produce some of their own nutrients) on roots of other flowering plants. Their main claim to fame lies in the genus Rafflesia, well-known as producers of the largest flowers in the world - Wikipedia gives the largest as over 100 cm in diametre and up to 10 kg in weight. I would be interested to know why they produce such ridiculously huge flowers. There just doesn't seem to be much point. When not flowering or fruiting, Rafflesiales are pretty much invisible, as they are otherwise entirely contained within the host.

I say "until very recently" because the Rafflesiales has, of recent years, fallen apart. This is not particularly surprising. Parasitic taxa of all varieties often show a great reduction in complexity, as organs related to nutrient gathering, production and processing lose their function - the host supplies all those things ready-made. Internal parasites are particularly notable in this regard. No need for a protective dermis of your own when you're safely contained within another organism's. No need for eyes, ears, nostrils - what are you going to see, hear, smell (that you would want to smell, at least)? Pretty much the only thing that the devoted endoparasite needs to do for itself is reproduce, and so many become little more than balls of gonad.*

*Seriously, no pun intended. I didn't even realise I'd written that at first.

Reduction in complexity often means loss of the characters that unite a parasitic clade with its non-parasitic sister group. And simplified characters come to resemble each other despite their different origins. Hence the previous unification of the families of 'Rafflesiales', and their sometimes-suggested connection with the Balanophorales, another group of reduced root-parasites (James Reveal seems to have phrased it best, though I'm not sure he meant quite the same thing as I do - "wherever go the Rafflesiales so go the Balanophorales").

The first molecular study that broke apart the Rafflesiales was Barkman et al. (2004). Barkman et al. looked at two genera of Rafflesiaceae (Rafflesia and Rhizanthes) as well as Mitrastema, another genus previously included in Rafflesiales. The two Rafflesiaceae clustered together, and appeared closely related to the Malpighiales, a large order of the flowering plant subclass Rosidae. In contrast, Mitrastema appeared as a member of the Ericales, in the subclass Asteridae. The remaining two families, Apodanthaceae and Cytinaceae, were added to the investigation by Nickrent et al. (2004). Cytinaceae was associated with Malvales (Rosidae). Apodanthaceae differed in its placement within Rosidae depending on which gene was examined, but it was never close to Rafflesiaceae (they may yet be related to Cytinaceae).

Nickrent et al. found that the peculiarities of 'rafflesialean' molecular evolution interfered with phylogenetic resolution. All the 'Rafflesiales' showed whacking great branch lengths, and when analysed under maximum parsimony, which is rather vulnerable to long-branch attraction (the tendency of long branches to randomly attach to each other), the Rafflesiales appeared as a near-monophlyetic clade. In one of the genes used by Nickrent et al., atp1, the Apodanthaceae clustered with Leguminosae, the host family of one of the Apodanthaceae. Because this result was in conflict with those from other genes, Nickrent et al. suggested that it represented lateral gene transfer from the host to the parasite. The occurrence of lateral (aka horizontal) gene transfer in eukaryotes is a subject of much debate, but it has been demonstrated to occur at least occasionally in flowering plants (Bergthorsson et al., 2003).

Most recently, Davis et al. (2007) investigated the specific position of Rafflesiaceae proper within Malpighiales, and found it to be actually nested within the Euphorbiaceae. This is a decidedly unexpected result, as Euphorbiaceae as a whole produce relatively minute flowers. Davis et al.'s result was unlikely to be simply long-branch attraction, because the other cluster on their tree to show accelerated evolutionary results was not Euphorbiaceae but the branch including Clusiaceae and Podostemaceae (the latter are aquatic plants that also show extreme reduction in complexity, to the point where they barely resemble flowering plants at all)*. I'm waiting in anticipation for Davis et al.'s results to be tested further.

*In recent years, there has been an increasingly distressing trend for articles to appear in high-impact journals with only the briefest of summaries of results in the actual printed journal, with the greater proportion of hard data, methods, etc. buried in online supplementary material (where it generally becomes inacessible after a couple of years). Davis et al. (2007) is actually one of the most extreme examples of this, with the printed article only a single page, with the supplementary info 424 pages long (fairness does compel me to admit that 415 pages of that are sequence alignments).

REFERENCES

Barkman, T. J., S.-H. Lim, K. Mat Salleh & J. Nais. 2004. Mitochondrial DNA sequences reveal the photosynthetic relatives of Rafflesia, the world's largest flower. Proceedings of the National Academy of Sciences of the USA 101 (3): 787-792.

Bergthorsson, U., K. L. Adams, B. Thomason & J. D. Palmer. 2003. Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature 424: 197-201.

Davis, C. C., M. Latvis, D. L. Nickrent, K. J. Wurdack & D. A. Baum. 2007. Floral gigantism in Rafflesiaceae. Science 315: 1812.

Nickrent, D. L., A. Blarer, Y.-L. Qiu, R. Vidal-Russell & F. E. Anderson. 2004. Phylogenetic inference in Rafflesiales: the influence of rate heterogeneity and horizontal gene transfer. BMC Evolutionary Biology 4: 40. (online here).