The evolution of hydrophobic cell wall biopolymers: from algae to angiosperms

Abstract

The transition from an aquatic ancestral condition to a terrestrial environment exposed the first land plants to the desiccating effects of air and potentially large fluctuations in temperature and light intensity. To be successful, this transition necessitated metabolic, physiological, and morphological modifications, among which one of the most important was the capacity to synthesize hydrophobic extracellular biopolymers such as those found in the cuticular membrane, suberin, lignin, and sporopollenin, which collectively reduce the loss of water, provide barriers to pathogens, protect against harmful levels of UV radiation, and rigidify targeted cell walls. Here, we review phylogenetic and molecular data from extant members of the green plant clade (Chlorobionta) and show that the capacity to synthesize the monomeric precursors of all four biopolymers is ancestral and extends in some cases to unicellular plants (e.g. Chlamydomonas). We also review evidence from extant algae, bryophytes, and early-divergent tracheophytes and show that gene duplication, subsequent neo-functionalization, and the co-option of fundamental and ancestral metabolic pathways contributed to the early evolutionary success of the land plants.

The Genome of the Charophyte AlgaPenium margaritaceumBears Footprints of the Evolutionary Origins of Land Plants

“…Neo- and subfunctionalization of catalytically promiscuous enzymes, including those in the ancient shikimate pathway (Niklas et al, 2017), would provide metabolic plasticity, which is associated with the evolution and functional diversification of phenylpropanoid compounds. However, the absence in the genome of P. margaritaceum and other charophytes of clear candidates for key steps in the pathway leading to various phenylpropanoid compound classes suggests the existence of cryptic activities and novel enzymes.…”

Insight into the physiological role of water absorption via the leaf surface from a rehydration kinetics perspective

“…Many nonvascular plants (e.g., many bryophytes) almost entirely rely on absorption of water through their aerial organs but frequently have external capillary conducting structures that hold only a well‐defined amount of water and leave much of the surface free for gas exchange (Dilks & Proctor, ). The evolution of vascular tissue and the development of a low‐resistance hydraulic path to supply water to leaves (leaf venation; Zwieniecki & Boyce, , Pittermann et al, ) allowed for evolution of epidermal structures, such as the cuticle (Niklas, Cobb, & Matas, ), stomata (Brodribb & McAdam, ), or trichomes (Brewer & Smith, ) that impact the exchange of matter in the solid (nutrients), liquid, and gas phase. However, more research is needed to shed light into the significance of leaf surface features in the context of whole‐leaf and whole‐plant function.…”

Surface Properties and Permeability to Calcium Chloride of Fagus sylvatica and Quercus petraea Leaves of Different Canopy Heights

“…The surface of the epidermal cells (also including trichomes or guard cells) of most aerial plant organs is covered with an extracellular layer named cuticle, that is laid down at early developmental stages ( Ingram and Nawrath, 2017 ; Petit et al, 2017 ). The cuticular membrane is traditionally defined as the non-living covering produced by the epidermis of some non-vascular land plants and the primary aerial organs of all vascular plants ( Niklas et al, 2017 ). More recently, it has become apparent that it is a specialized (but nevertheless integral) part of the primary cell wall ( Guzmán et al, 2014 ; Fernández et al, 2016 ), analogous in many regards to a lignified or a suberized secondary cell wall ( Niklas et al, 2017 ).…”

“…The cuticular membrane is traditionally defined as the non-living covering produced by the epidermis of some non-vascular land plants and the primary aerial organs of all vascular plants ( Niklas et al, 2017 ). More recently, it has become apparent that it is a specialized (but nevertheless integral) part of the primary cell wall ( Guzmán et al, 2014 ; Fernández et al, 2016 ), analogous in many regards to a lignified or a suberized secondary cell wall ( Niklas et al, 2017 ). This layer plays a crucial eco-physiological role when stomata are closed, and it is assumed that leaves of drought tolerant species may have a lower cuticular permeability than species from more mesic habitats ( Schuster et al, 2017 ).…”