Oxygen dynamics and plant-sediment interactions in isoetid ...

[Plant Signaling & Behavior 3:10, 882-884; October 2008]; ©2008 Landes BiosciencePaper 5Article AddendumOutstanding Lobelia dortmanna in iron armorKaj Sand-Jensen, Claus Lindskov Møller* and Ane Løvendahl RaunFreshwater Biological Laboratory; Biological Institute; University of Copenhagen; Hillerød DenmarkKey words: isoetids, Lobelia dortmanna, iron, ROL, sediment oxygen, iron plaquesLobelia dortmanna leads a group of small, highly-valued rosettespecies that grow on coarse, nutrient-poor soils in temperate softwaterlakes. They acquire most CO 2for photosynthesis by rootuptake and efficient gas transport in large air channels to the leaves.Lobelia is the only species that releases virtually all photosyntheticoxygen from the roots and generates profound day-night changes inoxygen and CO 2in the sediment pore-water. While oxygen releasefrom roots stimulates decomposition and supports VA-mycorrhizafungi, the ready gas exchange presents a risk of insufficient oxygensupply to the distal root meristems as sediments accumulate organicmatter from lake pollution. So the plant with the greatest oxygenrelease from roots is also the most sensitive to oxygen depletion insediments and it dies or losses anchorage by shortening the rootsfrom 10 to 2 cm at even modest contents (2.4%) of degradableorganic matter. Coatings of oxidized iron on roots in organicallyenriched sediments reduce radial oxygen loss and, thereby, increaseinternal concentrations and supply of oxygen to root tips. Oxidizediron is also a redox buffer which may prevent the ingress of sulfidesand other reduced toxic solutes during nights. Controlled experimentsare under way to test if iron enrichment can help survival ofrosette species threatened by lake pollution or whether removal oforganic surface sediments is required.Inhospitable SedimentsAquatic sediments and waterlogged soils are usually anoxic a fewmm below the surface. 1,2 Aquatic and wetland plants, therefore,need to supply oxygen to the roots by rapid intra-plant gas transportthrough large air channels running from the green shoot in contactwith atmospheric air or aerated water to the roots deeply buried inanoxic environments. 3,4 To ensure oxygen transport to the root tipin competition with radial oxygen loss to the anoxic hydrosoil, itshould be advantageous for roots to be thick, short and impermeableto radial oxygen loss. 5,6 Thick roots, however, are costly to producerelative to their capacity to take up nutrients so this morphology is*Correspondence to: Claus Lindskov Møller; Freshwater Biological Laboratory;Biological Institute; University of Copenhagen; Helsingørgade 51; Hillerød DE-3400Denmark; Email: clmoller@bio.ku.dkSubmitted: 06/26/08; Accepted: 06/26/08Previously published online as a Plant Signaling & Behavior E-publication:http://www.landesbioscience.com/journals/psb/article/6500Addendum to: Møller CL, Jensen KS. Iron plaques improve the oxygen supply to rootmeristems of the freshwater plant, Lobelia dortmanna. New Phytol 2008; 179:848–56; PMID: 18513220; DOI: 10.1111/j.1469-8137.2008.02506.x.not a general solution to cope with anoxic hydrosoils. Short roots,likewise, have a reduced nutrient uptake capacity and also a pooranchorage. Thus, the third option—having roots relatively impermeableto radial oxygen loss—appears to be a suitable solution. Indeed,this property is common among wetland plants, 6 it is present in themarine seagrass, Zostera marina and probably widespread amongmarine and freshwater plants (Fig. 1).Small freshwater rosette species, however, have highly gas permeableroot surfaces as an adaptation to take up free CO 2forphotosynthesis from the CO 2-rich hydrosoil in the nutrient-poorsandy sediments of softwater lakes. 1,7 These rosette species have thickentire leaves from a short stem, many roots and well-developed airchannels facilitating transport of oxygen and CO 2between leavesand roots. Utilizing CO 2from the hydrosoil for photosynthesis, theroots are also highly permeable to radial oxygen transport 8 and thisproperty has recently been confirmed by quantification of oxygenloss and root wall permeability for every 5 mm along the roots ofLobelia dortmanna. 9 The question therefore arises: how do thesespecies supply oxygen to root tips in sediments undergoing organicenrichment and oxygen depletion?Coping with Sediment Oxygen DepletionLobelia dortmanna is the only known species that releases virtuallyall photosynthetic oxygen from the roots to the sediments thanksto high root surface permeability and low leaf surface permeabilityand it, therefore, generates profound day-night fluctuations in poolsand penetration depth of oxygen in sandy sediments of low oxygenconsumption. 1,2 Sediment CO 2varies opposite to oxygen due totheir complementary roles in photosynthesis and respiration. 1 Otherrosette species also exchange much CO 2and oxygen via the roots, 8but leaf exchange is more important than in Lobelia.The ready oxygen exchange across Lobelia roots and the oxicconditions in nutrient-poor sediments have been regarded as anadvantage for the nutrient supply due to stimulation of organicdecomposition by aerobic sediment bacteria and mycorrhiza fungi. 1This situation is reversed, however, in sediments undergoing organicenrichment by input from the catchment or from phytoplankton-richlake water. Organically enriched sediments of higher oxygen demandoffer a threat to survival of rosette species due to higher radial oxygenloss and insufficient oxygen supply to root tips during the night whenphotosynthetic oxygen production is switched off and the lake wateris the only oxygen source to plant and sediment respiration. 7,9Organic enrichment of sandy Lobelia sediments leads to a declinein root length from about 10 cm to 2 cm (Fig. 2). While growth and882 87Plant Signaling & Behavior 2008; Vol. 3 Issue 10