Symbiosis in cycads: the origin and development of coralloid roots in Macrozamia communis (Cycadaceae)

Coralloid roots of Macrozamia have more apparent developmental stages than those of many other cycad genera, providing an ideal study vehicle for obtaining a better understanding of the growth and development of symbiotic cycad coralloid roots. In M. communis L. Johnson, the process begins with initiation of young apogeotropic, papillose roots called “precoralloids” and involves phases of maturation, cyanobacterial invasion, coralloid formation, senescence, and regeneration. Active precoralloid apices continue to produce papillose tissue, but during precoralloid maturation, the prominent papillose sheath is gradually replaced by a thin, dermal layer with scattered lenticels. Cyanobacterial invasion has been observed at different stages of precoralloid maturation and stimulates further, irreversible development of precoralloids into coralloids. Newly invaded precoralloids in the process of transition may be readily identified by their distinctive apical lenticels. Coralloid development involves transformation of the original, apogeotropic precoralloid tissue as well as production of new coralloid tissue by apical meristems. Although continuous, these two coralloid regions may be recognized by their external morphology. New coralloid growth involves cessation of papillose sheath production, change in gravitropic response, proliferation of lenticels, and early differentiation of a conspicuous cyanobacterial zone. Three mechanisms enabling continuity of the coralloid root system are: 1) production of new precoralloids and coralloids from bases of existing roots of the same kind; 2) initiation of atypical roots from within the internal tissues of degenerating coralloids; and 3) development of internal secondary periderm during decortication of aging coralloid tissue.