This Botanical Briefing reviews how the integration of palaeontology, geochemistry and developmental …

• Abstract
• Introduction
• Evolution of the leaf and atmosphere
• Genes, leaves and stomata
• Vegetation feedbacks and the long-term carbon cycle
• Conclusions
• Literature cited
• Figures

Biology Articles » Evolutionary Biology » Leaf Evolution: Gases, Genes and Geochemistry » Introduction

Introduction

- Leaf Evolution: Gases, Genes and Geochemistry

Plants evolved leaves on at least two independent occasions and the legacy of these historic evolutionary events is represented in extant floras by microphylls in lycophytes (clubmosses, spikemosses and quillworts) and megaphylls in euphyllophytes (ferns, gymnosperms and angiosperms). Microphylls, with a distinctive vasculature and (usually) unbranched venation, are thought to have evolved from spine-like enations and predate megaphylls in the terrestrial plant fossil record (Gifford and Foster, 1988). Of greater significance, however, was the origin of megaphylls in vascular plants through the developmental modification of lateral branches. Megaphylls altered the evolutionary trajectory of terrestrial plant and animal life, the biogeochemical cycling of nutrients, water and carbon dioxide and the exchange of energy between the land surface and the atmosphere. The vast majority of the estimated 250 000 or so extant species of flowering plants, as well as most gymnosperms and (extinct) pteridosperms, utilize(d) a flat-bladed megaphyll with a network of veins to capture solar energy for photosynthetic carbon assimilation. A true measure of their success in terrestrial environments is the capacity of leaves to endure climatic extremes between the tropics and the tundra whilst simultaneously facilitating the global scale net fixation of approx. 207 billion tonnes of CO₂ (56·4 x 10¹⁵ g C) year^–1 (Field et al., 1998). This primary production provides energy for virtually all forms of terrestrial life on Earth, especially tetrapods and insects, and links many ecosystem and biogeochemical processes.

Evidently, leaves are a global success. However, the advent of large megaphylls took place some 40–50 million years (Myr) after the origination of vascular land plants, suggesting that they were far from an evolutionary inevitability. The earliest ancestral vascular plants, dating to the late Silurian 410 Myr ago (Edwards and Wellman, 2001), were composed of simple or branched axial stems with sporangia but no leaves. Surprisingly, plants continued to remain leafless for the next 40–50 Myr, with megaphylls finally becoming widespread at the close of the Devonian period (360 Myr ago) (Kenrick and Crane, 1997; Boyce and Knoll, 2002; Osborne et al., 2004a,b). Surprise in the delayed appearance of a seemingly simple developmental modification is 3-fold. First, palaeontological evidence shows that the structural framework necessary for assembling a simple laminated leaf blade (meristem, vasculature, cuticle and epidermis) (Kenrick and Crane, 1997) was in place long before the advent of large megaphylls. Secondly, the same interval marks an unparalleled burst of evolutionary innovation in the history of plant life, which witnessed the rise of trees from herbaceous ancestors, and the evolution of complex life cycles, including the seed habit (Kenrick and Crane, 1997). Thirdly, the tiny deeply incised megaphylls of the rare early-Devonian plant Eophyllophyton bellum from Chinese rocks shows that plants had the capacity to produce a simple megaphyll (Hao and Beck, 1993; Hao et al., 2003). Why were plants unable to release this morphogenetic potential?

Until recently, our understanding of the evolution of megaphylls largely stemmed from Zimmermann's telome theory (Zimmermann, 1930, 1952) describing the sequence of overtopping, planation and webbing leading to appearance of the laminated leaf blade. The ancestral form of a dichotomizing axis branching out in three dimensions and typified by the rhyniophytes (Fig. 1) represents the basal state in the telome theory. Evolutionary ‘overtopping’ followed producing a main axis bearing reduced, lateral, determinate photosynthetic stems, branching out in three dimensions (e.g. trimerophytes). These 3-D lateral branch systems of terete stem segments then became ‘flattened’ into a single plane (e.g. cladoxyaleans). Finally, a webbing of photosynthetic mesophyll tissue joined the flattened segments of the lateral branches to form a laminate leaf blade (e.g. some progymnosperms) (Fig. 1). In this scheme, transformation of a branch into a leaf was achieved by simple modification of existing organs rather than a major change in body plan.

 
Over 70 years ago, Zimmermann's scholarly telome theory provided a first glimpse of the ‘how’, but left unanswered the thorny question of ‘why’ it took 40–50 Myr to evolve leaves. This Botanical Briefing provides an overview of a new mechanistic explanation linking atmospheric CO₂ decline with the delayed widespread appearance of megaphylls, and ideas concerning its molecular genetic basis and the resulting global environmental and evolutionary consequences. The explanation emerges from a theoretical analysis incorporating modern-day plant processes and biophysical principles governing the energy balance of photosynthetic organs (Beerling et al., 2001). Developmental genetic mechanisms underpinning aspects of stomatal and leaf formation (Gray et al., 2000; Cronk, 2001; Floyd and Bowman, 2004; Harrison et al., 2005; Sano et al., 2005) provide additional new insight allowing progress towards a unified framework for understanding leaf evolution. In the final section of this Briefing, I consider how recognizing a role for CO₂ in leaf evolution has shed new light on multiple biotic feedbacks within the geochemical carbon cycle and on evolutionary processes themselves (Oddling-Smee et al., 2003; Beerling and Berner, 2005).