The cellular cortex in Collemataceae (lichenized Ascomycota) participates in thallus growth and morphogenesis via parenchymatous cell divisions

ABSTRACT

According to a widely held view, fungi do not produce parenchymatous tissues. Following up on recent transmission electron microscopy (TEM) evidence that challenged this paradigm in several lichens, we employed scanning electron microscopy (SEM) to investigate the orientation of new anticlinal walls in the single-layered fungal cortex of six species of Collemataceae, a family of gelatinous cyanolichens with diverse surface morphologies. Examination of thallus surfaces in four species of Leptogium (L. austromericanum, L. burnetiae, L. chloromelum, L. marginellum) and two species of Scytinium (S. gelatinosum, S. lichenoides) revealed that recently formed septa adjoin to preceding septa in parenchymatous division. These cortical divisions were evident in the formation and development of thallus wrinkles, folds, isidia, and lobules in the six morphologically distinct taxa. Tomentum, by contrast, arose as filamentous outgrowths of the cortical cells. We conclude that the monostromatic cellular cortex in Collemataceae participates in surface growth and morphogenesis by means of parenchymatous cell divisions, in a remarkable parallel to plant meristems. Cortical cell divisions do not appear to drive morphogenesis, however, as very similar morphologies are achieved in the closely related genus Collema, which lacks a cortex altogether. These results provide evidence that parenchymatous cell division can indeed play a role in morphogenesis of fungal structures and show that SEM is a useful tool for distinguishing the orientation of anticlinal divisions in the cortex of gelatinous lichens.

KEYWORDS:

• Collema
• fungal tissue
• Leptogium
• lichen cortex
• lichen thallus
• parenchyma
• parenchymatous division
• pseudoparenchyma
• plectenchyma
• Scytinium
• septation

ACKNOWLEDGMENTS

Technical assistance with SEM was kindly provided by Alberto Jorge and Marta Furió (Museo Nacional de Ciencias Naturales, CSIC). We thank Dr. Isaac Garrido-Benavent for helpful discussions and assistance with collections in the field. The manuscript benefited from critical review by several anonymous referees.

Additional information

Funding

Funding was provided by a Spanish Ministry of Economy and Competitiveness grant (CTM2015-64728-C2-2-R to A.d.l.R.).