Hugh Dickinson on a new article in Science that sheds more light on the Alternation of the Generations. When does a diploid plant decide to become a haploid?
Anyone who has sat in a botany class from high school onwards will be familiar with the idea of the ‘Alternation of Generations’. In this botanical circle of life both lower (ferns and mosses) and flowering plants oscillate between a haploid (one set of chromosomes) ‘gametophyte’ generation – big in lower plants, reduced to a few cells in flowering plants – and a diploid (2 sets of chromosomes) ‘sporophyte’ generation – small in lower plants, the ‘main plant’ in higher plants. The gametophyte (haploid) generation – be it big or small – generates the sex cells (pollen and eggs in flowering plants). These then get together to form the diploid sporophyte which, in turn, produces the gametophytes – D.C.al fine (as they say in musical scores).
The gametophyte to sporophyte switch occurs when the sperm and egg snuggle up to form a zygote, but when the switch from sporophyte to gametophyte takes place is not clear. The purists would have it that this conversion happens when the products of meiosis (spores) divide to form pollen or embryosacs in flowering plants, ‘prothalli’ in ferns and the main plant bodies of mosses and liverworts. But what of meiosis – the process by which the genetical die is cast for the subsequent haploid generation that follows? Certainly cells of the sporophyte contribute to meiosis, but the spectacular nuclear events that occur in the meiotic lineage, during which genes are exchanged between chromosomes, somehow belong neither to the sporophyte or gametophyte and exist in some sort of intergenerational limbo.
Whatever (a good word for accepting that botanists will never agree about some things), we remain depressingly ignorant about the switching system that decides when a sporophytic cell lineage dividing happily by mitosis, suddenly develops an interest in sex, ‘goes meiotic’ and forms the gametophyte. Most agree that the control of this switch – which the plant certainly does not want to throw by mistake – is likely to be pretty complicated and to involve more than one gene system – analogous to the ‘dual key’ systems for launching nuclear Armageddon (but with arguably less dramatic consequences).
This certainly seems to be the case. An international group of scientists led by Arp Schnittger in Hamburg and published in Science has just unravelled the control mechanism for making sure that, in the female lineage of the model plant Arabidopsis, only one cell enters the meiotic pathway. Even this simple step requires interaction between a total of 3 gene systems (1) the WUSCHEL (WUS) gene family which regulates cell proliferation in all plant meristems, (2) The RETINOBLASTOMA-LIKE 1 (RBR1) gene pathway which manages the shutting down of the cell cycle and halts cell division at the right point, and (3) three members of the KIP RELATED PROTEIN (KRP) gene family which seem to run the show and make sure that things occur at the right place and time. When this system goes off the rails, more than one of the normal single female meiotic cells (aka the ‘megaspore mother cell (MMC)’) are formed; for example, in the triple KRP mutant, 2 of these cells develop, and in the RBR1 mutant many MMCs are formed, all crowded together in the developing ovule – the female sex organ in higher plants (see images below). Although these multiple MMCs undergo meiosis and turn into embryo sacs that can attract pollen tubes, no fertilisation takes place suggesting that the system runs aground later in development.
Does any of this matter in the grand scheme of things? Yes, it certainly does. One of the main R&D targets for the plant biotechnology industry is to be able to produce ‘apomictic’ seed that is genetically identical to its mother plant (not having had its genes recombined by the meiotic ‘one arm bandit’). Arp Schnittger and his colleagues now have their hands on the system that controls entry to the very first stage in the female development and – if they can tweak it to produce a mitotic rather than a meiotic cell – their way will be open to generate single or multiple diploid embryo sacs. OK, pollination is normally required both to add a paternal nucleus and ‘boot’ seed development, but there are processes in some plants where this can be bypassed. Bringing these systems together could result in a technology which would transform the plant breeding industry.
Hugh Dickinson is Emeritus Professor of Plant Reproductive Biology (and chairman of the Annals of Botany Company). His research concentrates on the cell biology, genetics and epigenetic programming of reproductive cell (germ-cell) lineages.
Zhao, X., Bramsiepe, J., Van Durme, M., Komaki, S., Prusicki, M. A., Maruyama, D., … Schnittger, A. (2017). RETINOBLASTOMA RELATED1 mediates germline entry in Arabidopsis. Science, 356(6336), eaaf6532. https://doi.org/10.1126/science.aaf6532