THE EVOLUTION OF PARASITISM IN RED ALGAE: CELLULAR INTERACTIONS OF ADELPHOPARASITES AND THEIR HOSTS¹

Abstract

In the initial stages of cell–cell interactions (spore germination and host penetration), the adelphoparasites Gardneriella tuberifera Kyl. and Gracilariophila oryzoides Setch. & Wilson form infection rhizoids that fuse directly with underlying host epidermal or cortical cells. In so doing, parasite nuclei and other organelles enter the cytoplasm of the host. The resulting heterokaryon may fuse with adjacent host cells either directly, via secondary pit connections, or by the dissolution or dislodgment of pit plugs from existing pit connections. The cell fusion events result in a heterokaryotic syncytium in which parasite nuclei replicate. In Gardneriella, formation of the syncytium induces surrounding host tissues to divide to form a photosynthetic callus. The internalized syncytium forms conjunctor and rhizoidal cells that fuse with host callus, eventually transforming the host callus into cells containing parasite nuclei. Gracilariophila does not induce surrounding host tissue to divide. Rather, division of the initial heterokaryotic tissue gives rise to the colorless mantle that protrudes from the host and forms reproductive structures. The heterokaryotic tissue also fuses with underlying host cells, thereby spreading parasite nuclei throughout adjacent host cells. In both these adelphoparasites, transformation of host cells by parasite nuclear invasion results in plastid dedifferentiation, an increase in mitochondria, autolysis of organelles, and accumulation of large amounts of floridean starch. The development and physiology of these parasites is similar to normal post‐fertilization processes in the hosts that give rise to carposporophytes and suggests that these adelphoparasites may have originated from perturbations of developmental pathways involved in their host's post‐fertilization development.

What's in a name? Monophyly of genera in the red algae: Rhodophyllis parasitica sp. nov. (Gigartinales, Rhodophyta); a new red algal parasite from New Zealand

“…This suggests that 2nd pit connections are an essential feature not only of the early developmental stages of the parasite (Zuccarello et al 2004) but are also essential for parasite-host development (Goff andColeman 1985, Zuccarello andWest 1994). 2nd pit connections allow the parasite to transfer nuclei and cytoplasmic organelles to host cells (Goff and Coleman 1984) and appear to give the parasite control over the host cells (Goff and Coleman 1987); the parasite changes the metabolism within the infected host cells and transforms the morphology of host cells (Goff and Zuccarello 1994). Even though 2nd pit connections were observed between the parasite and R. membranacea, changes in host cell morphology were not observed.…”

“…Another important character are the presence of secondary pit connections (2nd PC) formed between parasite and host cells (Goff 1982). 2nd PC have been observed in nearly all described red algal parasites studied (e.g., Fredericq and Hommersand 1990, Goff and Zuccarello 1994, Goff and Coleman 1995.…”

Are all red algal parasites cut from the same cloth?

“…Once a parasite spore lands upon a susceptible host, the parasite carpospore (2N) or tetraspore (1N) will germinate and undergo an initial cell division [21]. Adelphoparasite cells will divide between 1 and 3 more times before one of the cells forms a rhizoid that penetrates the surface of the host, growing into the wall of a host epidermal cell [21]. The tip of the rhizoid swells isolating a single parasite nucleus along with its organelles into a conjunctor cell which divides from the infection rhizoid [21,22].…”

“…Adelphoparasite cells will divide between 1 and 3 more times before one of the cells forms a rhizoid that penetrates the surface of the host, growing into the wall of a host epidermal cell [21]. The tip of the rhizoid swells isolating a single parasite nucleus along with its organelles into a conjunctor cell which divides from the infection rhizoid [21,22]. This conjunctor cell then fuses, via a secondary pit connection, with the adjacent host cell (Fig.…”

Epulo multipedes gen. et sp. nov. (Corallinaceae, Rhodophyta), a coralline parasite from Australia

“…These de scriptions were essentially morphological (e.g. Goff 1982;Goff & Zuccarello 1994;Zuccarello & West 1994;Broad water & Lapointe 1997;Chamberlain 1999) and it was not until the latter years of the century that the evolutionary re lationships between parasite and host and between parasites were examined using molecular tools (Goff et al 1996(Goff et al , 1997.…”