Occurrence and phylogenetic significance of glucose utilization by charophycean algae: glucose enhancement of growth in Coleochaete orbicularis

Abstract

Two critical innovations had a profound influence upon the evolutionary history of plants: the nutritionally dependent embryo and apoplastic phloem loading processes. Both depend upon the ability of the plant cell membrane to transport sugars. The evolutionary origin of sugar transport by plants is, therefore, of special phylogenetic importance. Recent evidence suggests that hexoses such as glucose are the main form of sugar transported apoplastically across the placental junction between gametophyte and sporophyte of the moss Polytrichum (Renault et al., 1992, Plant Physiology 100: 1815–1822). There is also considerable evidence that hexose transport may be involved in apoplastic phloem loading in Arabidopsis and other flowering plants. Results of numerous molecular, biochemical, immunofluorescence, and ultrastructural studies indicate that bryophytes and charophycean algae are related to the ancestors of vascular plants. This report demonstrates that the charophyte Coleochaete orbicularis exhibits enhanced growth in the presence of glucose under conditions in which inorganic carbon sources are limiting. Computer image analysis was used to demonstrate that nonaerated cultures of C. orbicularis grown for 7 weeks in an inorganic medium supplemented with 1% glucose produce as much as 13.6 times the biomass of clonal cultures grown for the same length of time in the same medium without glucose. Furthermore, addition of 1% glucose to nonaerated cultures yielded chlorophyll a concentration 20 times higher after 4 weeks growth than cultures grown under the same conditions without added glucose. This and other evidence derived from comparative growth measurements strongly suggest that Coleochaete takes up (or loads) glucose. Experimental results also suggest that hexose uptake by charophytes (such as Coleochaete) that typically grow in low alkalinity waters might provide a supplementary source of organic carbon when dissolved carbon dioxide levels are low. This capability could have served as an evolutionary precursor to hexose import by plant embryos, as well as leptom and phloem loading in bryophytes and vascular plants.