Who Would Have Thought? Biggest Flower, Biggest Gene Thief

by Elio

Fully opened flower of Rafflesia arnoldii from the Palupu Reserve near Bukittinggi, Indonesia. Photo by Troy Davis. Source.

Rafflesias in the tropical rain forests of Southeast Asia produce some of the biggest flowers in the world—up to one meter in diameter. Adding to their notoriety is their carrion-like smell to attract insects for pollination service. They’re not microbes by anyone's definition of the term. The reason they make an appearance in these pages is that they have stolen a larger proportion of their genome via horizontal gene transfer (HGT) than any other organism we know of. Between 24% and 41% of their mitochondrial DNA is of foreign origin, and even in their nucleus a whopping 2.1% of the genes were imported.

Plant genomes seem to be especially rife in genes acquired by HGT, and this is particularly true for the parasitic kinds, of which the Rafflesias are impressive examples. These freeloaders have no leaves or stems, no plastids anywhere—thus no photosynthesis. They live off host vines whose nutrients they harvest via haustoria, absorptive organs that penetrate into the host’s tissues. These un-plantlike plants exist concealed within their host vines, only occasionally offering a showy reproductive structure to the outer world—reminiscent of the mushrooms formed by underground fungal mycelia. Now we have learned that they are not only trophic parasites, but also genomic thieves.

Rafflesias and their host lineages diverged approximately 115 million years ago, which makes it easy to distinguish the transferred genes. During that time, the Rafflesias lost their photosynthetic organelles, so they offer no plastid DNA for study. Instead, the authors selected for investigation 38 mitochondrial genes that are found in most angiosperms, including both those coding for proteins and for ribosomal RNA. They compared these genes from two species of Rafflesia, one species from another closely-related genus, and three species of host vines (Vitaceae) using au courant transcriptomics, next-generation sequencing, and complementary data analysis. Most of the multitude of mitochondrial genes transferred to Rafflesia are intact and are actively transcribed. Many are in clusters that maintain their original order (synteny), thus suggesting acquisition by homologous recombination.

Moreover, the authors envision that these exchanges took place without the intervention of transposable elements, bacteria, or viruses, in other words, without any of the Small Things that we typically invoke as agents of HGT. How about that, biology can be exciting even without involving microbes!

How to account for this massive unidirectional gene theft? One can surmise that the intimate association of parasitic Rafflesias with their hosts facilitated this enormous amount of direct gene transfer. Thus we can expect that other parasitic plants (mistletoes, Indian pipes, broomrapes, dodder) will soon be subjected to similar scrutiny. Wouldn’t this have profound consequences all around the Tree of Life?

Zhenxiang Xi, Yuguo Wang, Robert K. Bradley, M. Sugumaran, Christopher J. Marx, Joshua S. Rest,, & Charles C. Davis (2013). Massive Mitochondrial Gene Transfer in a Parasitic Flowering Plant Clade PLoS Genetics, 9 (2) DOI: 10.1371/journal.pgen.1003265

Comments

[Mark O. Martin]

Is this more kleptogenomic than our rotifer friends, Elio?

http://www.sciencemag.org/content/320/5880/1210.abstract

Maybe so. But this all just tells me that the natural world exchanges genetic information in an almost perversely promiscuous fashion! I used to tell students that HGT among prokaryotes puts Hollywood promiscuity to shame; it's like someone have children by their Caesar salad.

Maybe this plant is still more shameless?

Thanks again for such great material to discuss in class with my students!