Two distinct fungi colonize roots and rhizomes of the myco-heterotrophic Afrothismia gesnerioides (Burmanniaceae)

Abstract

The subterranean organs of Afrothismia gesnerioides H. Maas consist of short rhizomes densely covered with ovoid root tubercles, each of which may extend into a short filiform root extension. Serial sections revealed the presence of two distinct fungi occupying different niches within the plant tissues. Rhizomes and roots are divided into separate compartments hosting different morphotypes of the aseptate, exclusively intracellular hyphae of fungus A: (i) straight and persistent hyphae in the root epidermis, root extension, and outer rhizome cortex, (ii) coiled but still persistent hyphae in the third root layer, (iii) coiled hyphae undergoing degeneration in the root cortical parenchyma, (iv) starch depositions in the inner rhizome cortex and no colonization by fungus A, and (v) a partly collapsed root hypodermis serving as compartment barrier. The colonization by fungus A is interpreted as an aberrant arbuscular mycorrhiza of the Paris type. The compartmentation allows the separation of tissues where the hyphae stay functional from those in which the fungal material is digested. This pattern may represent a complex but efficient strategy for a sustained benefit from the few fungal penetrations that occur. Comparison with earlier work on Afrothismia winkleri (Engl.) Schltr. revealed considerable differences between the mycorrhizae that are interpreted as evolutionary steps. There are signs that these changes even may have improved the mycorrhizal benefit for the plant. The monomorphic hyphae of fungus B are smaller in diameter, septate, grow inter- as well as intra-cellularly, but are always characteristically appressed to the inner cell walls. It does not change its appearance within the root/rhizome compartments as does fungus A. Neither hyphal degeneration nor interferences with fungus A, starch depositions, or alterations in the development of A. gesnerioides could be noticed. Fungus B possibly is a commensal, but relevance to the symbiosis cannot be ruled out.