Biggest Flower, Biggest Gene Thief

Who Would Have Thought?

by Elio

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 – ac­cord­ing to Xi et al. (2013) – 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.

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

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?