The origin of alternation of generations in land plants: a focus on matrotrophy and hexose transport

A life history involving alternation of two developmentally associated, mul ticellular generations (sporophyte and gametophyte) is an autapomorphy of e mbryophytes (bryophytes + vascular plants). Microfossil data indicate that Mid-Late Ordovician land plants possessed such a life cycle, and that the o rigin of alternation of generations preceded this date. Molecular phylogene tic data unambiguously relate charophycean green algae to the ancestry of m onophyletic embryophytes, and identify bryophytes as early-divergent land p lants. Comparison of reproduction in charophyceans and bryophytes suggests that the following stages occurred during evolutionary origin of embryophyt ic alternation of generations: (i) origin of oogamy; (ii) retention of eggs and zygotes on the parental thallus; (iii) origin of matrotrophy (regulate d transfer of nutritional and morphogenetic solutes from parental cells to the next generation); (iv) origin of a multicellular sporophyte generation; and (v) origin of non-flagellate, walled spores. Oogamy, egg/zygote retent ion and matrotrophy characterize at least some modern charophyceans, and ar e postulated to represent pre-adaptative features inherited by embryophytes from ancestral charophyceans. Matrotrophy is hypothesized to have preceded origin of the multicellular sporophytes of plants, and to represent a crit ical innovation. Molecular approaches to the study of the origins of matrot rophy include assessment of hexose transporter genes and protein family mem bers and their expression patterns. The occurrence in modern charophyceans and bryophytes of chemically resistant tissues that exhibit distinctive mor phology correlated with matrotrophy suggests that Early-Mid Ordovician or o lder microfossils relevant to the origin of land plant alternation of gener ations may be found.