bs_bs_banner Plant, Cell and Environment (2015) 38, 1737–1751 doi: 10.1111/pce.12458 Review Sphagnum physiology in the context of changing climate: emergent influences of genomics, modelling and host–microbiome interactions on understanding ecosystem function David J. Weston1, Collin M. Timm1, Anthony P. Walker2, Lianhong Gu2, Wellington Muchero1, Jeremy Schmutz3,4, A. Jonathan Shaw5, Gerald A. Tuskan1, Jeffrey M. Warren2 & Stan D. Wullschleger2 1Biosciences Division and 2Environmental Sciences Division and Climate Change Science Institute, Oak Ridge National Laboratory, Oak Ridge, TN 37831, USA, 3Department of Energy Joint Genome Institute, Walnut Creek, CA 94598, USA, 4HudsonAlpha Institute of Biotechnology, Huntsville, AL 35806, USA and 5Department of Biology, Duke University, Durham, NC 27708, USA ABSTRACT INTRODUCTION Peatlands harbour more than one-third of terrestrial carbon Almost one-third of all soil organic carbon is stored in north- leading to the argument that the bryophytes, as major com- ern peatland ecosystems – an estimated 455 to 547 Gt C in ponents of peatland ecosystems, store more organic carbon in boreal bogs, fens and tundra wetlands (Gorham 1991; Yu soils than any other collective plant taxa. Plants of the genus 2012). Peatlands cover 400 million ha throughout the North- Sphagnum are important components of peatland ecosystems ern Hemisphere and develop when net photosynthetic CO2 and are potentially vulnerable to changing climatic condi- fixation (net primary production or NPP) exceeds all forms tions. However, the response of Sphagnum to rising tempera- of biomass loss (e.g. decomposition, erosion, wild fire) for tures, elevated CO2 and shifts in local hydrology have yet to be thousands of years, resulting in the formation and accumula- fully characterized. In this review, we examine Sphagnum tion of peat deposits that can be tens of metres thick (Rydin biology and ecology and explore the role of this group of & Jeglum 2006; Limpens et al. 2008). This pool of stored keystone species and its associated microbiome in carbon and organic carbon, much of it in a form that could be made nitrogen cycling using literature review and model simula- readily available to microbial degradation, is vulnerable to tions. Several issues are highlighted including the conse- globally rising temperatures, changes in local hydrology, quences of a variable environment on plant–microbiome increased occurrence and severity of wildfires and other dis- interactions, uncertainty associated with CO2 diffusion resist- turbance regimes (McGuire et al. 2009). Current net flux of ances and the relationship between fixed N and that parti- carbon to the atmosphere as CO2 and CH4 from northern tioned to the photosynthetic apparatus. We note that the peatlands is estimated to be 276 Tg C annually and could Sphagnum fallax genome is currently being sequenced and increase to 473 Tg C per year by the end of the century outline potential applications of population-level genomics (Zhuang et al. 2006). Changes in the carbon balance of and corresponding plant photosynthesis and microbial meta- peatlands could provide a positive feedback to atmospheric bolic modelling techniques. We highlight Sphagnum as a forcing of climate if these ecosystems and their component model organism to explore ecosystem response to a changing organisms were to be destabilized by climatic change, land climate and to define the role that Sphagnum can play at the use or disturbance (Turetsky et al. 2012). intersection of physiology, genetics and functional genomics. Sphagnum peat mosses are keystone species in peatland ecosystems and therefore exert a substantial impact on eco- Key-words: bryophyte; climate change; genetics; nitrogen system function and net carbon (C) balance across the land- fixation; mosses; peatlands. scape (Clymo & Hayward 1982; Gorham 1991; Wieder 2006). Although several hundred species of Sphagnum exist, only a Correspondence: D. J. Weston. Fax: +865 576 9939; e-mail: westondj few dozen that are known to greatly influence ecosystem @ornl.gov function have been studied within the context of physiology This paper has been co-authored by UT-Battelle, LLC, under Con- and environmental variation. It is well known that different tract No. DE-AC05-00OR22725 with the US Department of Energy. Sphagnum species spatially organize along topographic gra- The US Government retains and the publisher, by accepting the dients with water chemistry, pH, water table depth and article for publication, acknowledges that the US Government retains a non-exclusive, paid-up, irrevocable, worldwide license to surface moisture content as strong drivers of species distri- publish or reproduce the published form of this manuscript, or allow bution (Titus & Wagner 1984; van Breemen 1995; Hajkova & others to do so, for US Government purposes. Hajek 2007). Field observations such as these have been © 2014 The Authors. Plant, Cell & Environment published by John Wiley & Sons Ltd. 1737 This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes. 1738 D. J. Weston et al. confirmed in greenhouse and growth chamber studies, control the supply of water for maintaining function. The where interspecific competition is evident in the response of unique contribution of plant–microbe interactions to the Sphagnum to water table, precipitation and temperature carbon and nitrogen cycle in Sphagnum is described and a (Robroek et al. 2007a,b). Because climate, hydrology, nitro- preliminary model is offered to potentially link these two gen deposition and disturbance can have dramatic conse- frontiers. Finally, a strategy is presented where the sequenc- quences for plant community composition (Berendse et al. ing of the Sphagnum genome could complement and expand 2001) and the concomitant CO2 and CH4 fluxes (Strom et al. genetic and physiological insights for bryophyte plant 2003; Koelbener et al. 2010), it is critical that the nature and, species. where possible, the genetic basis for Sphagnum growth, interspecific competition, plasticity and resilience be deter- SPHAGNUM POPULATION STRUCTURE AND mined (Turetsky et al. 2012). GENETIC DIVERSITY Multiple lines of evidence suggest that the distribution of Sphagnum species across environmental gradients is associ- As in other mosses, the Sphagnum life cycle includes two ated with physiological function. Poikilohydric plants (i.e. stages that potentially result in dispersal and gene flow.Sperm plants that cannot actively regulate their water uptake and is released into the environment by the paternal gametophyte loss), such as Sphagnum species, lack cuticle and stomata that and requires water to reach an egg. The zygote develops into regulate water loss (Titus et al. 1983); additionally, Sphagnum an unbranched sporophyte that consists of little more than a species lack roots for soil water extraction. Therefore, pro- sporangium, within which meiotic spores are produced. cesses, such as photosynthesis, depend on the passive main- Sphagnum gametophytes can be either monecious, producing tenance of tissue water content through the capillary uptake both egg and sperm, or dioecious. Gametophyte sexuality is of water up from the water table, precipitation inputs and generally a fixed species characteristic,although a few species, water storage by the plant. Sphagnum species have repeat- especially in the Sphagnum subgenus Acutifolia, appear to be edly been shown to achieve maximum photosynthetic rates hermaphroditic (Crum 1984). Of the 91 species of Sphagnum across a broad range of tissue water contents (600 to 3400% that occur in North America, 14 are known to have dioecious dry mass) that decline rapidly with drought and desiccation gametophytes, 58 have monecious gametophytes and the rest (Titus et al. 1983; Murray et al. 1989; Schipperges & Rydin have unknown sexual conditions (McQueen & Andrus 1996). 1998; Maseyk et al. 1999). Recovery of physiological function Species with dioecious gametophytes have high levels of following desiccation also appears to be an interspecific intragametophytic selfing (which yields a completely attribute, but has been studied in only limited detail homozygous sporophyte in one mating episode), although (Schipperges & Rydin 1998; Robroek et al. 2009). Addition- some outcrossing also occurs (Johnson et al. 2012).Monecious ally, there are indications that Sphagnum photosynthesis is species have mixed mating systems with varying degrees of sensitive to low temperatures, but that high rates of photo- inbreeding. There are important interactions between synthesis may be maintained at temperatures up to 30 °C or microhabitat (elevated hummocks versus lower hollows) and higher (Harley et al. 1989; Hanson et al. 1999; Haraguchi & mating patterns. An analysis of 14 species showed that Yamada 2007). Recently, the influence of temperature has inbreeding coefficients were higher in dioecious hummock been extended to include effects on plant–microbe interac- populations than in dioecious hollow populations, but the tions, food web dynamics and nitrogen cycling within Sphag- opposite was true for monecious species: hummock popula- num peatlands (Jassey et al. 2013). Admittedly, knowledge of tions had lower inbreeding coefficients than hollow popula- individual and combined effects of increased temperature tions (Johnson et al. 2012).Sporophytic inbreeding