Abstract
Low-oxygen stress, mainly caused by soil flooding, is a serious abiotic stress affecting crop productivity worldwide. To understand the mechanisms of low-oxygen stress responses and adaptation of plants, we characterized and compared low-oxygen responses in six species with different accessions of the Brassicaceae family. Based on the growth and survival responses to submergence or low-oxygen condition, these accessions could be divided into three groups: (i) Highly tolerant species (Rorippa islandica and Arabis stelleri); (ii) moderately tolerant species (Arabidopsis thaliana [esk-1, Ler, Ws and Col-0 ecotype]); and (iii) intolerant species (Thlaspi arvense, Thellungiella salsuginea [Shandong and Yukon ecotype], and Thellungiella parvula). Gene expression profiling using Operon Arabidopsis microarray was carried out with RNA from roots of A. thaliana (Col-0), A. stelleri, R. islandica, and T. salsuginea (Shandong) treated with low-oxygen stress (0.1% O2/99.9% N2) for 0, 1, 3, 8, 24, and 72 h. We performed a comparative analysis of the gene expression profiles using the gene set enrichment analysis (GSEA) method. Our comparative analysis suggested that under low-oxygen stress each species distinctively reconfigures the energy metabolic pathways including sucrose–starch metabolism, glycolysis, fermentation and nitrogen metabolism, tricarboxylic acid flow, and fatty acid degradation via beta oxidation and glyoxylate cycle. In A. thaliana, a moderately tolerant species, the dynamical reconfiguration of energy metabolisms occurred in the early time points of low-oxygen treatment, but the energy reconfiguration in the late time points was not as dynamic as in the early time points. Highly tolerant A. stelleri appeared to have high photosynthesis capacity that could produce more O2 and in turn additional ATP energy to cope with energy depletion caused by low-oxygen stress. R. islandica seemed to retain some ATP energy produced by anaerobic energy metabolism during a prolonged period of low-oxygen conditions. Intolerant T. salsuginea did not show significant changes in the expression of genes involved in anaerobic energy metabolisms. These results indicate that plants developed different energy metabolisms to cope with the energy crisis caused by low-oxygen stress.
Highlights
Plant growth and development is highly dependent on a variety of environmental conditions such as temperature, light, water availability, and soil conditions
Gene sets associated with photosynthesis, major CHO metabolism, mitochondrial electron transport/ATP synthesis, and miscellaneous group were enriched in T. salsuginea, while gene sets associated with gluconeogenese/glyoxylate cycle, metal handling, auxin metabolism, tetrapyrrole synthesis, biotic stress, biodegradation of xenobiotics, C1 metabolism, transcription factor and protein were enriched in A. thaliana (Figure 3C and Supplementary Table S4)
In A. thaliana, the dynamical reconfiguration of energy metabolisms in early response was restricted in late response to low-oxygen stress, suggesting that the survival of A. thaliana is seriously affected when exposed to a low-oxygen condition for a prolonged period
Summary
Plant growth and development is highly dependent on a variety of environmental conditions such as temperature, light, water availability, and soil conditions. Gene sets associated with photosynthesis, major CHO metabolism, mitochondrial electron transport/ATP synthesis, and miscellaneous group were enriched in T. salsuginea, while gene sets associated with gluconeogenese/glyoxylate cycle, metal handling, auxin metabolism, tetrapyrrole synthesis, biotic stress, biodegradation of xenobiotics, C1 metabolism, transcription factor and protein were enriched in A. thaliana (Figure 3C and Supplementary Table S4) These results suggest that in low-oxygen conditions, T. salsuginea activates the energy-generating metabolic pathways, rather than defense mechanisms, which might make T. salsuginea very sensitive to low-oxygen stress. Positively enriched gene sets were associated with gluconeogenese/glyoxlate cycle, protein and transport, and negatively enriched gene sets were associated with photosynthesis, glycolysis, OPP pathway, cell wall, amino acid metabolism, C1 metabolism, DNA, signaling and development These results indicated that major anaerobic metabolic pathways in T. salsuginea such as fermentation and glycolysis were highly altered by low-oxygen stress. The root temperature of R. islandica and A. stelleri, highly tolerant species, increased 3.5 °C and 1.5 °C by lowfooxry1g2enhs, trreesspsefcotriv1e2lyh,, wrehspileectthiveerleyw, wahs inleotshiegrneifiwcaasnnt ochsiagnngieficianntthcehraonogtetienmtpheerraotoutreteomfpAe.rathtualrieanoaf aAn.dthTa.lisaanlsauagnindeaT(.Fsiaglusuregi5nAea–C(F)i.gHuorew5eAve,Br,,Cth)e. iHr hoiwghevteerm, ptheeriartuhriegshdteecmrepaesreadturraepsiddleycrweahseenderxappoisdeldy twohneonrmexaplogsreodwtothncoornmdaitligornosw(Fthigcuorned5iCtio).nTsh(eFitgeumrepe5rCa)t.uTreheintcermeapseersatauftreerinlocwre-aosxeysgaefntesrtlroewss-ooxnylygeinn bstortehsshoignhlytoinlerbaontthshpiegchietso(lRer.aisnltansdpieccaieasnd(RA. .issltaenlldeircia) iamnpdliAed. stthelaletrtih) eimhepalitemd itghhattbtehegehneeartamteidghfrtobme ugepnreegrautleadtiofrnoomf fuerpmreegnutlaattiioonn aocftivfeitrimeseuntnadtieornhyacptoivxiitciecsonudnidtieornshyinpothxeicsechonigdhittioonlesrainnt tshpeesceiehs,igahs itmolperliacnattesdpebcyieosu, arsmimicrpoliacrartaeydrbeysuoltusr. microarray results
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