Of Crosses and Clubs

One of the major groups of eukaryotes that has been somewhat under-represented on this site has been the Cercozoa. This is a diverse clade of unicellular organisms, distantly related to the foraminiferans and radiolarians, that has only been recognised within the last few decades with the introduction of molecular phylogenetic analyses. It has become increasingly clear that cercozoans form a major part of the world's microscopic biota but this diversity is poorly known as most cercozoans have little direct effect on human industry. One subgroup of the cercozoans that does make itself known in this regard, however, is the Phytomyxea.

Club roots of a rape plant infected by Plasmodiophora brassicae, photographed by Leafhopper65.

The Phytomyxea include parasites of plants, algae and other aquatic micro-organisms. The best known phytomyxean species, Plasmodiophora brassicae, causes a condition known as 'club root' in cabbages; another, Spongospora subterranea, is responsible for powdery scab on potatoes. They form multinucleate 'plasmodia' when growing within the cells of their host. Nuclei divide within the plasmodium in a characteristic cruciform pattern: the nucleolus does not break down during division but instead stretches elongately before pinching in two. While stretched, the nucleolus is oriented perpendicularly to the separating chromatin, forming a cross (Dylewski 1990). Owing to a superficial resemblance between phytomyxean plasmodia and those formed by the plasmodial slime moulds, phytomyxeans were historically also treated as slime moulds and hence as fungi (alternative historical names for the group, such as Plasmodiophoromycota or Plasmodiophoromycetes, reflect this supposed affinity). However, whereas the amoeboid plasmodia of slime moulds are capable of active movement and ingestion of food particles via phagocytosis, the phytomyxean plasmodium is more or less incapable of moving of its own volition, instead moving within the host cell by means of the host's own cytoplasmic streaming, and do not engulf host tissue in vacuoles. Slime moulds are no longer regarded as a single evolutionary lineage, and no 'slime moulds' are directly related to fungi.

Nuclei undergoing cruciform division in plasmodium of Tetramyxa parasitica, copyright James P. Braselton.

Over 40 species of Phytomyxea have been recognised to date but, not surprisingly, studies on the group have focused heavily on those species of economic importance to humans (Neuhauser et al. 2011). Terrestrial phytomyxeans produce thick-walled resting cysts, often aggregated in clumps known as cystosori, that may persist in soil for several years. These cysts hatch into biflagellate primary zoospores that seek out a suitable host. Upon finding one, the spore ceases swimming and adheres to the host cell before piercing the cell wall and injecting its cytoplasm which grows into the aforementioned plasmodium. Nuclei divide by mitosis and are eventually parcelled into sporangia that release secondary zoospores that escape from the host cell. These secondary spores generally do not disperse far; instead, they tend to cycle back and re-infect the original host to form new plasmodia. When these secondary plasmodia reach maturity, their nuclei divide meiotically and are divvied into new resting cysts. Presumably, the haploid nuclei produced in this manner fuse at some point with another to return to diploidy but it is unknown when exactly this happens. The cysts, when formed, each contain two nuclei but later only one, so it is possible that this reduction results from fusion. However, it might seem more likely that one of the nuclei breaks down without issue and the cyst remains haploid through to excystment with fusion occurring at the primary zoospore phase, thus allowing greater scope for cross-fertilisation. Marine phytomyxeans have long been thought not to produce resting cysts but recent observations of variations in zoospore morphology and sporangial wall thickness in the brown algal parasite Maullinia ectocarpii suggest the possibility of similarly complex life cycles (Neuhauser et al. 2011). The length of the phytomyxean life cycle can vary from about a month for Plasmodiophora brassicae to as little as one or two days for the brown algal parasite Phagomyxa algarum.

Diagram of the life cycle of Plasmodiophora brassicae, from Auer & Ludwig-Müller (2015).

For most phytomyxean species, infection by plasmodia causes physiological changes in the host, commonly taking the form of galls or other excesses of growth. Club root disease of Brassica results from Plasmodiophora brassicae plasmodia producing growth hormones that cause nutrients to be concentrated in the roots at the expense of leaf growth, thus increasing their availability to the parasite. Other alterations may be related to parasite dispersal. Ligniera junci, a parasite of rushes, causes a proliferation in the growth of root hairs in which the resting cysts form, providing an extra protective sheath. Plasmodiophora bicaudata is a parasite of marine Zostera eelgrass that produces galls at internodes together with reduced root growth. As a result, the eelgrass is easily uprooted by water movement, potentially being carried to new areas where the next generation of phytomyxeans can find new eelgrasses to infect.

REFERENCES

Dylewski, D. P. 1990. Phylum Plasmodiophoromycota. In: Margulis, L., J. O. Corliss, M. Melkonian & D. J. Chapman (eds) Handbook of Protoctista. The structure, cultivation, habitats and life histories of the eukaryotic microorganisms and their descendants exclusive of animals, plants and fungi. A guide to the algae, ciliates, foraminifera, sporozoa, water molds, slime molds and the other protoctists pp. 399–416. Jones & Bartlett Publishers: Boston.

Neuhauser, S., M. Kirchmair & F. H. Gleason. 2011. The ecological potentials of Phytomyxea ("plasmodiophorids") in aquatic food webs. Hydrobiologia 659: 23–35.