Bacterial leaf symbiosis in Dioscorea sansibarensis: morphology and ultrastructure of the acuminate leaf glands*

Abstract

The symbiosis between a bacterium and the West African rain forest yam Dioscorea sansibarensis is described for the first time at the ultrastructural level. The bacteria are harboured in glands which run the entire length of the pronounced ‘drip‐tip’ leaf acumenae of the host plant. Each acumen, which may be up to 12 cm long in very large mature leaves, contains from two to six bacterial glands. The glands are kidney‐shaped in cross section and contain numerous multicellular simple trichomes which arise from the epidermis of the gland floor and project into the lumen of the gland. The bacteria are Gram‐negative and variously rod, ovoid, and coccoid in shape. The bacterial cells contain mesosomes, polyhydroxybutyrate granules and large electron‐dense bodies. Bacteria‐free plants grow more slowly and produce one yellowish‐green leaf per node in contrast to the vigorous growth habit of infected plants, with two deep green leaves per node. Infected plants exposed to a variety of atmospheres containing acetylene, both in the light and in the dark, failed to reduce acetylene to ethylene, indicating that nitrogen fixation is not a function of this symbiosis.

The Potato Yam Phyllosphere Ectosymbiont Paraburkholderia sp. Msb3 Is a Potent Growth Promotor in Tomato

“…D. sansibarensis is considered the only species of the monocot family, in which nodule formation occurs (Carlier et al, 2017;Pinto-Carbo et al, 2018;De Meyer et al, 2019), however, the genomic similarity between our strain and O. dioscoreae (Carlier et al, 2017), their position and abundance on the leaf and the role of secretory trichomes (Miller and Reporter, 1987;Pinto-Carbo et al, 2018) as well as the close phylogenetic relationship of both hosts (Viruel et al, 2018) and microbes (Carlier et al, 2017) are indicative for conserved structures mediating these associations. Both symbionts are bona fide epiphytes for at least part of their life (Carlier et al, 2017) and form clusters on secretory trichomes on the leaf acumen (Miller and Reporter, 1987) of their true yam host plant. In light of the absence of nodules in D. bulbifera our findings could be interpreted as an early stage in the development of such a structure.…”

“…Trichomes develop into the bacteria-filled lumen. They are thought to play a role in the exchange of nutrients (Miller and Reporter, 1987;Carlier et al, 2017).…”

Bacterial leaf glands in Styrax camporum (Styracaceae): first report for the family

“…The role of the mucilage in the nourishment of bacteria and in their transportation, enabling the infection of the leaves and seeds of the host plants, has been discussed previously (Lersten and Horner 1967;Whitmoyer and Horner 1970;Miller et al 1983;Miller and Reporter 1987;Van Oevelen et al 2003). In the three plant families that maintain bacterial leaf symbioses, the bacterial colony resides in the stem apical region, which is permanently filled with the mucilage secreted by specialized trichomes (dendroid colleters in Rubiaceae, Miller et al 1983;stellate trichomes in Myrsinaceae, Miller et al 1984;multicellular trichomes in Dioscoreaceae, Miller and Reporter 1987).…”

“…In the two nodulated dicotyledonous families, leaf nodules are initiated in the shoot tip during the early stages of leaf development by the entry of bacteria-laden mucilage through the stomata (Rubiaceae) or hydathodes (Myrsinaceae), and the bacteria are in close contact with the internal tissues of the host plant (Miller et al 1983). In the Dioscoreaceae, bacteria are harbored in ducts formed by the invagination of the adaxial epidermis of the leaf acumen lined with secretory trichomes, and the bacteria are being held out of the host plant tissue (Miller and Reporter (1987). In S. camporum, the glands are a constitutive trait, originating in the early stages of leaf development, and all of the glands are colonized with bacteria during the mature stage.…”

Bacterial Leaf Nodule Symbiosis in Flowering Plants

“…In Ardisia and Psychotria, evidence showed that if the associated bacteria were lost (or decrease to a limit amount, see below), the shoot tip would loss normal function, degenerated to callus (called "cripple" symptom or phenotype), and eventually died within a few years [25,26,[30][31][32]. The symptom suggests that the endosymbionts may be responsible for plant normal growth and development, probably by producing hormonal substances.…”