An Or­chid, Two Fungi

by Roberto

What do you do when you have a headache? Per­haps you ob­tain re­lief by tak­ing a pill, maybe ac­eta­minophen, maybe ibupro­fen. Thanks to the won­ders of mod­ern med­i­cine, we can tend to nu­mer­ous ail­ments with a panoply of syn­thetic com­pounds, i.e., phar­ma­ceu­ti­cals. But, if you fol­low Tra­di­tional Chi­nese Med­i­cine, your treat­ment of headaches, as well as other mal­adies like ver­tigo and dizzi­ness, would no doubt in­clude the widely used "Tian ma." The use of this med­i­c­i­nal herb goes back more than 2000 years; it is doc­u­mented in the Shen­nong Ben­cao­jing, the clas­sic com­pi­la­tion of Chi­nese med­i­c­i­nal plants writ­ten around the first cen­tury. Tian ma is the com­mon name for the tu­ber of the or­chid Gas­tro­dia elata.

Be­fore div­ing deeper into the fas­ci­nat­ing life cy­cle of G. elata, here's a very brief primer on or­chids. The or­chid fam­ily of plants (Or­chi­daceae) is very large. It is thought to rep­re­sent about 10% of all seed plants and con­tains in the or­der of 30,000 species. Within the stun­ning di­ver­sity of this fam­ily, there are sev­eral shared char­ac­ter­is­tics among its mem­bers. Quite no­tably, their seeds are ex­tremely small. Thus, the em­bryo has vir­tu­ally no nu­tri­ents to grow on. In­stead, to ini­ti­ate growth, or­chids of­ten need the help of other or­gan­isms. This is where the mi­cro­bi­ol­ogy of or­chids gets in­ter­est­ing. To ger­mi­nate, most or­chid seeds must land on or very near fungi and then es­tab­lish an in­ti­mate re­la­tion­ship where the fun­gus pro­vides most nu­tri­ents. This de­pen­dency of the plant on a fun­gus is known as my­co­heterotro­phy. Most or­chids are fac­ul­ta­tive my­co­heterotrophs. They even­tu­ally turn on pho­to­syn­the­sis and be­come au­totrophs. But not G. elata.

Gas­tro­dia elata. Source

As plants go, G. elata has some un­ex­pected fea­tures. Above ground, it con­sists of a sin­gle stem with flow­ers at its tip. But it does not de­velop any branches or leaves. Most strik­ingly, there is noth­ing green about this plant. It never makes any chloro­phyll, no pho­to­syn­the­sis. What? Is this re­ally a plant? No leaves, no branches, no pho­to­syn­the­sis? What kind of a plant is this? G. elata takes my­co­heterotro­phy to the ex­treme, it is an ob­lig­ate my­co­heterotroph. The bulk of this plant's mass is un­der­ground. But, com­ple­ment­ing its above-ground odd­ity, it has no ma­jor root sys­tem. Rather, the or­chid forms a sin­gle large tu­ber, the source of Tian ma.

The life cy­cle of Gas­tro­dia elata. Mycena is es­sen­tial for the stage de­noted by the red ar­rows, Armil­laria is nec­es­sary for the stage de­picted by the green ar­rows, no fungi are re­quired for the stages in­di­cated by the blue ar­rows. Source

It takes around three years for G. elata to com­plete its life cy­cle. I sug­gest this re­view as an ex­cel­lent read to get at the nitty gritty de­tails of how this cy­cle is de­pen­dent on the es­tab­lish­ment of in­ti­mate as­so­ci­a­tions with two dif­fer­ent fungi. Here I will sum­ma­rize some of this orchid's de­vel­op­ment that I find most fas­ci­nat­ing. First, to ger­mi­nate, the seeds must en­counter a fun­gus of the genus Mycena. This is a rare event in nat­ural set­tings; it is no won­der that a sin­gle G. elata plant will pro­duce sev­eral mil­lion of these tini­est of seeds. The Mycena fungi pro­vide the sig­nals needed for seed ger­mi­na­tion and the nu­tri­ents for the ini­tial veg­e­ta­tive growth of the plant. But de­vel­op­ment stops there. The plant en­ters an ini­tial dor­mancy that lasts some four months. Then, a sec­ond fun­gus comes into the scene that pro­vides the nu­tri­ents re­quired for the for­ma­tion of im­ma­ture tu­bers. Af­ter a sec­ond dor­mancy pe­riod, this sec­ond fun­gus again pro­vides the nu­tri­ents for the de­vel­op­ment of ma­ture tu­bers. Af­ter yet a third dor­mancy, and us­ing the nu­tri­ents from the tu­ber, the sin­gle stem emerges. The life cy­cle is com­pleted with the for­ma­tion of flow­ers, pol­li­na­tion, and seed de­vel­op­ment.

I must ad­mit that it was the na­ture of the sec­ond fun­gal sym­biont that drew my at­ten­tion to this or­chid. It was none other that Armil­laria gal­lica! Why does this ex­cite me so? Well, A. gal­lica and closely re­lated species are well-known for an­other rea­son. In­di­vid­u­als can get very old and very large. These fea­tures were pop­u­lar­ized by the gifted writer and evo­lu­tion­ary bi­ol­o­gist Stephen Jay Gould in his de­light­ful 1992 es­say "A Hu­mungous Fun­gus Among Us," pub­lished in Nat­ural His­tory Mag­a­zine. (The whole of the 1992 vol­ume is down­load­able from the AMNH Dig­i­tal Li­brary. Within that vol­ume, search for is­sue 7, page 10 and en­joy the read!)

Some Armil­laria in­di­vid­u­als com­pete for be­ing among the biggest, heav­i­est, and old­est in­di­vid­u­als on Earth. One found in east­ern Ore­gon is thought to cover ten square kilo­me­ters, weigh some­where be­tween 7,000 and 35,000 tons, and may be up­wards of 8,000 years old. Armil­laria achieve fast growth and ef­fec­tive pre­da­tion by bundling many in­di­vid­ual hy­pha into root-like threads, rhi­zomorphs. Long-time STC fans might re­mem­ber Elio's post on Armil­laria de­scrib­ing its gar­gan­tuan di­men­sions.

Armil­laria in­vades the veg­e­ta­tive prop­a­ga­tion corm of G. elata. Epi­der­mal cells (A). Pelo­ton cells (B). Sus­cep­ti­ble fun­gal cell ©. Di­ges­tive cells (D). Rhi­zomorph (E). Outer sheath (F). Mem­brane (G). Hy­phae (H). The hy­phal chan­nel (I). Hy­phal flow (J). Pap­il­lary pro­tru­sion (K). Pelo­ton (L). Hy­phal frag­ments (M). Source

Back to G. elata. What is the Hu­mungous Fun­gus do­ing on this de­vel­op­ing or­chid. This is yet an­other ex­am­ple of an in­tri­cate two-way chem­i­cal ex­change process be­tween dif­fer­ent species. The or­chid se­cretes phy­to­hor­mones such as strigo­lac­tones that are sensed by the fun­gus as an at­trac­tant. Us­ing the strength pro­vided by its large rhi­zomorphs, along with di­ges­tive en­zymes, the fun­gus bores into the de­vel­op­ing or­chid by break­ing through the epi­der­mis (out­er­most layer). Once in the cor­tex, the rhi­zomorph dis­so­ci­ates and hy­phae pen­e­trate in­di­vid­ual "fun­gal-sus­cep­ti­ble" cells. 

From here on­wards the en­dosym­bio­sis reaches a fas­ci­nat­ing equi­lib­rium. In­side some of the cor­ti­cal cells the hy­phae grow as coils (called pelo­tons, prob­a­bly be­cause of the sim­i­lar­ity to groups of cy­clists...). If such growth were to con­tinue un­abated, the or­chid would suf­fer. In­stead, the or­chid con­trols the fun­gal in­fec­tion. First, through the ac­tion of gas­tro­di­an­ins, small an­ti­fun­gal pro­teins. Sec­ond and more im­por­tantly, some of the plant's cor­ti­cal cells turn into di­ges­tive cells, where the fun­gal pelo­tons are com­pletely de­graded, pro­vid­ing the plant all the nu­tri­ents it needs for tu­ber growth.

Of course, there's a lot more to these in­ter­ac­tions than these two part­ners. Where does the fun­gus ob­tain its nu­tri­ents? As any self-re­spect­ing sapro­phyte, from de­cay­ing leaf mat­ter and dead trees. Armil­laria rhi­zomorphs can also in­vade liv­ing trees and slowly kill them. So, the hu­mungous fun­gus can be killing a tree in one place while, at a very dis­tant lo­ca­tion, it is di­gested by a de­vel­op­ing or­chid, giv­ing the plant nu­tri­ents to grow its tu­ber. A tu­ber which, in turn, may some­day be dug out and in­gested by a hu­man to re­lieve a mal­ady. A hu­man, who, in time, might plant a tree... Mul­ti­par­tite sym­bioses know no end!