The Size of Cells and Organisms in Relation to the Evolution of Embryophytes

Abstract

The earliest O₂-evolvers were marine cyanobacteria (3.5 billion years ago) with marine eukaryotic phototrophs from 2.0 billion years ago. These organisms were, and are, poikilohydric, i.e., cannot remain hydrated when exposed to a desiccating atmosphere (as can occur for intertidal benthic algae and cyanobacteria at low tide). The smallest marine primarily poikilohydric O₂-evolvers are close to the lower size limit imposed by non-scaleable components such as minimum genome size and constant membrane thickness, with cyanobacterial unicells 0.65 µm in diameter and eukaryotic unicells 0.95 µm in diameter. The largest (multicellular) marine primarily aquatic poikilohydric O₂-evolvers are brown algae at least 60 m long and over 100 kg fresh mass; there are no obvious constraints on the maximum size of such organisms. In freshwaters the size range for primarily poikilohydric O₂-evolving organisms is smaller, due to the absence of very large organisms. An even smaller size range characterizes terrestrial algae and cyanobacteria which have occurred for about 1 billion years. Desiccation-tolerant cyanobacterium and algae (intertidal, freshwater, terrestrial) are at the lower end of the size ranges.

Embryophytic terrestrial O₂-evolvers arose some 450 million years ago and were than all poikilohydric and (probably) desiccation-tolerant. Embryophytic defining structural features require organisms of at least 100 µm equivalent spherical diameter for both gametophyte and sporophyte phases. Primarily poikilohydric embryophytes are not more than 1 m tall as a result of a mechanistically mysterious size limit for desiccation-tolerant organisms. Homoiohydric embryophytes evolved some 420 million years ago in the sporophyte phase (later to become the dominant terrestrial vegetation) and possibly in the gametophyte phase (although no such homoiohydric gametophytes are known today). The homoiohydric features of gas spaces, stomata, cuticle, endohydric water conducting system and water and nutrient uptake structures require an organism at least 5 mm high; this has implications for the minimum size of megaspores and seeds. The tallest homoiohydric plants are (or were within historic times) 130 m high, with height constrained by resource costs of the synthesis and maintenance of the mechanical and water conduction systems, and/or of xylem water transport. Secondarily poikilohydric embryophytes in aquatic, or very damp terrestrial, habitats are derived from homoiohydric plants; they retain most homoiohydric features but are not functionally homoiohydric. The smaller secondarily poikilohydric plants are less than one tenth of the size of the smallest functionally homoiohydric plants.

Key Words

Desiccation-intolerance - desiccation-tolerance - eukaryotes - homoiohydry - poikilohydry - prokaryotes