Title: Oxygen Sensing Coordinates Photomorphogenesis to Facilitate Seedling Survival
Abstract: Successful emergence from the soil is essential for plant establishment in natural and farmed systems. It has been assumed that the absence of light in the soil is the preeminent signal perceived during early seedling development, leading to a distinct morphogenic plan (skotomorphogenesis) [1Wu S.H. Gene expression regulation in photomorphogenesis from the perspective of the central dogma.Annu. Rev. Plant Biol. 2014; 65: 311-333Crossref PubMed Scopus (78) Google Scholar], characterized by traits providing an adaptive advantage until emergence and photomorphogenesis. These traits include suppressed chlorophyll synthesis, promotion of hypocotyl elongation, and formation of a closed apical hook that protects the stem cell niche from damage [2Abbas M. Alabadí D. Blázquez M.A. Differential growth at the apical hook: all roads lead to auxin.Front. Plant Sci. 2013; 4: 441Crossref PubMed Scopus (84) Google Scholar, 3Mazzella M.A. Casal J.J. Muschietti J.P. Fox A.R. Hormonal networks involved in apical hook development in darkness and their response to light.Front. Plant Sci. 2014; 5: 52Crossref PubMed Scopus (65) Google Scholar]. However, absence of light by itself is not a sufficient environmental signal for early seedling development [4Sperling U. van Cleve B. Frick G. Apel K. Armstrong G.A. Overexpression of light-dependent PORA or PORB in plants depleted of endogenous POR by far-red light enhances seedling survival in white light and protects against photooxidative damage.Plant J. 1997; 12: 649-658Crossref PubMed Scopus (119) Google Scholar, 5Raz V. Ecker J.R. Regulation of differential growth in the apical hook of Arabidopsis.Development. 1999; 126: 3661-3668Crossref PubMed Google Scholar]. Reduced oxygen levels (hypoxia) can occur in water-logged soils [6Crawford R.M.M. Oxygen availability as an ecological limit to plant distribution.in: Advances in Ecological Research. Volume 23. Academic Press, 1992: 93-185Google Scholar, 7Liptzin D. Silver W.L. Detto M. Temporal dynamics in soil oxygen and greenhouse gases in two humid tropical forests.Ecosystems. 2011; 14: 171-182Crossref Scopus (129) Google Scholar, 8Silver W.L. Lugo A.E. Keller M. Soil oxygen availability and biogeochemistry along rainfall and topographic gradients in upland wet tropical forest soils.Biogeochemistry. 1999; 44: 301-328Google Scholar]. We therefore hypothesized that below-ground hypoxia may be an important, but thus far undiscovered, ecological component regulating seedling development. Here, we show that survival and establishment of seedlings following darkness depend on their ability to sense hypoxia, through enhanced stability of group VII Ethylene Response Factor (ERFVII) transcription factors. Hypoxia is perceived as a positive environmental component in diverse taxa of flowering plants, promoting maintenance of skotomorphogenic traits. Hypoxia greatly enhances survival once light is perceived, while oxygen is necessary for the subsequent effective completion of photomorphogenesis. Together with light perception, oxygen sensing therefore allows an integrated response to the complex and changing physical microenvironment encountered during early seedling growth. We propose that plants monitor the soil’s gaseous environment after germination, using hypoxia as a key external cue to protect the stem cell niche, thus ensuring successful rapid establishment upon emergence above ground.