274 Review Article Formation of Aerenchyma and the Processes of Plant Ventilation in Relation to Soil Flooding and Submergence M. B. Jackson 1 and W. Armstrong2 1 IACR-Long Ashton Research Station, Department of Agricultural Sciences, University of Bristol, Long Ashton, United Kingdom 2 Department of Biological Sciences, University of Hull, Hull, United Kingdom Received: November 12, 1998; Accepted: February 22, 1999 Abstract: Enhanced development of gas-spaces beyond that due to the partial cell separation normally found in ground parenchymas and their derivatives creates tissue commonly termed "aerenchyma". Aerenchyma can substantially reduce internal impedance to transport of oxygen, nitrogen and var- ious metabolically generated gases such as carbon dioxide and ethylene, especially between roots and shoots. Such transport lessens the risk of asphyxiation under soil flooding or more complete plant submergence, and promotes radial oxygen loss from roots leading to oxidative detoxification of the rhizo- sphere. Aerenchyma can also increase methane loss from wa- terlogged sediments via plants to the atmosphere. This review of the formation and functioning of aerenchyma particularly emphasises research findings since 1992 and highlights pros- pects for the future. Regarding formation, attention is drawn to how little is known of the regulation and processes that create schizogenous aerenchyma with its complex cell arrangements and differential cell to cell adhesion. More progress has been made in understanding lysigenous aerenchyma development. The review highlights recent work on the processes that sense oxygen deficiency and ethylene signals, subsequent transduc- tion processes which initiate cell death, and steps in protoplast and wall degeneration that create the intercellular voids. Simi- larities between the programmed cell death and its causes in animals and the predictable patterns of cell death that create lysigenous aerenchyma are explored. Recent findings concern- ing function are addressed in terms of the diffusion aeration of roots, rhizosphere oxygenation and sediment biogeochemistry, photosynthesis and ventilation, pressurised gas-flows and greenhouse gas emissions and aspects of ventilation related to secondary thickening. Key words: Aerenchyma, anaerobiosis, apoptosis, environmen- tal stress, ethylene, gas transport, plant aeration, pressure flow, programmed cell death, review, roots, water plants. Plant biol. 1(1999) 274—287 © Georg Thieme Verlag Stuttgart. New York ISSN 1435-8603 Introduction Cell to cell diffusion over short distances across tissues pro- vides constituent cells with environmental oxygen or carbon dioxide needed for aerobic respiration and photosynthesis. It also enables them to discharge unwanted volatiles such as ethylene, methyl jasmonate, salicylic acid and ethanol. Such cell by cell aeration, in gas or liquid, is usually serviced by near- by interfaces with an external air phase. However, when these interfaces are eliminated by inundation, the submerged organs risk asphyxiation. In species well-adapted to flooding, the risk is minimised by internal long-distance apoplastic gas trans- port pathways of low impedance created by a continuum of gas-filled aerenchyma (e.g., in Avecennia marina, Ashford and Allaway, 1995]211). This allows better aerated plant parts to be used as remote intake- or exhalation-vents for the benefit of remote inundated organs. Such pathways are an addition to the gas space continuum of higher impedance that permeates ground tissues of root, root-shoot junctions and shoots of most vascular plants (Armstrong, l9791'). A convenient defining feature that distinguishes aerenchymatous from non-aeren- chymatous tissue is that in the former, facing sides of adjacent cells become parted as a result of cell separation or the col- lapse of intervening cells. Many wetland species form aeren- chyma constitutively in roots, leaves and stems while others, including certain amphibious and land plants, initiate or in- crease the extent of aerenchyma in response to poor aeration (e.g., Watkin et al., 199811481). Aerenchyma can take a variety of forms, some of which are both structurally complex and me- chanically strong despite their small tissue mass (Arber, 192012]; Sculthorpe, 196711211; Justin and Armstrong, 1987185]). The extent to which a permeating aerenchyma can satisfy di- rectly the need for oxygen by metabolically active growing points such as root apices when their surroundings are anaero- bic, depends on many factors. Of particular significance are temperature, the longitudinal path length involved and the oxygen demand along it, the availability of photosynthetic oxygen (Pederson et al., 19951108]) and the duration or period- icity of submergence (Skelton and Alloway, 199611271). As well as acting in ventilation, aerenchyma may also serve as an oxy- gen reservoir in submerged plants (Gaynard and Armstrong, 1987163]) and improve their buoyancy. The mechanisms that maintain the intercellular spaces gas-filled rather than water- filled are not fully understood (Raven, 199611121) but are a fea- ture of living tissue and thus appear to be metabolically main-