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Complex regulatory network allows Myriophyllum aquaticum to thrive under high-concentration ammonia toxicity.

ABSTRACT: Plants easily experience ammonia (NH₄⁺) toxicity, especially aquatic plants. However, a unique wetland plant species, Myriophyllum aquaticum, can survive in livestock wastewater with more than 26?mM NH₄⁺. In this study, the mechanisms of the M. aquaticum response to NH₄⁺ toxicity were analysed with RNA-seq. Preliminary analysis of enzyme activities indicated that key enzymes involved in nitrogen metabolism were activated to assimilate toxic NH₄⁺ into amino acids and proteins. In response to photosystem damage, M. aquaticum seemed to remobilize starch and cellulose for greater carbon and energy supplies to resist NH₄⁺ toxicity. Antioxidative enzyme activity and the secondary metabolite content were significantly elevated for reactive oxygen species removal. Transcriptomic analyses also revealed that genes involved in diverse functions (e.g., nitrogen, carbon and secondary metabolisms) were highly responsive to NH₄⁺ stress. These results suggested that a complex physiological and genetic regulatory network in M. aquaticum contributes to its NH₄⁺ tolerance.

SUBMITTER: Wang R

PROVIDER: S-EPMC6423053 | biostudies-literature | 2019 Mar

REPOSITORIES: biostudies-literature

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Complex regulatory network allows Myriophyllum aquaticum to thrive under high-concentration ammonia toxicity.

Wang Rui R Xu Shengjun S Sun Haishu H Feng Shugeng S Jiang Cancan C Zhou Sining S Wu Shimin S Zhuang Guoqiang G Chen Baodong B Bai Zhihui Z Zhuang Xuliang X

Scientific reports 20190318 1

Plants easily experience ammonia (NH4+) toxicity, especially aquatic plants. However, a unique wetland plant species, Myriophyllum aquaticum, can survive in livestock wastewater with more than 26 mM NH4+. In this study, the mechanisms of the M. aquaticum response to NH4+ toxicity were analysed with RNA-seq. Preliminary analysis of enzyme activities indicated that key enzymes involved in nitrogen metabolism were activated to assimi ...[more]

PMID: 30886354

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Project description:Background and aimsThe mature morphology of most plants can usually be said to consist of three mutually exclusive organs: leaves, stems, and roots. The vast majority of mature morphologies may be easily grouped into one of these mutually exclusive categories. However, during very early stages of development and in many instances from inception, the division between organ categories becomes fuzzy due to the overlap in developmental processes that are shared between the aforementioned mutually exclusive categories. One such overlap has been described at the gene level where KNOXI homologues, transcription factors responsible for maintaining indeterminate cell fate, are expressed in the shoot apical meristem and during early stages of compound leaf development. This study characterizes the occurrence and spatial localization of mRNA of a KNOXI homologue, MaKN1, during the early stages of development in the simple leaves of Myriophyllum aquaticum, an aquatic angiosperm from the family Haloragaceae exhibiting pentamerous whorls of finely lobed leaves.MethodsA 300-bp KNOXI fragment was sequenced from M. aquaticum and used in an RNA localization study to determine the temporal and spatial expression of KNOXI during the early stages of leaf lobe development in M. aquaticum. The developmental sequence of leaves of M. aquaticum was also described using scanning electron microscopy.Key resultsLobe development of M. aquaticum occurs in two very distinct regions at the leaf base in an alternating fashion reminiscent of a distichous shoot system. It was discovered that MaKN1 expression is localized to both the shoot apical meristem and early stages of leaf primordia development (P1-P7). Initially, MaKN1 is expressed ubiquitously throughout primordia (P1-P3); however, as lobes develop, MaKN1 becomes localized to recently emerged lobe primordia, and disappears as lobes develop basipetally.ConclusionsThe pattern of gene expression is indicative of shared developmental processes during early development between shoots, compound leaves, highly lobed simple leaves and unifoliate simple leaves which lack KNOXI expression. These findings are supportive of Arber's less rigid 'partial shoot' theory, which conceptualizes compound leaves as having shoot-like elements.

Project description:Ammonia (NH3) inhibition represents a major limitation to methane production during anaerobic digestion of organic material in biogas reactors. This process relies on co-operative metabolic interactions between diverse taxa at the community-scale. Despite this, most investigations have focused singularly on how methanogenic Archaea respond to NH3 stress. With a high-NH3 pre-adapted and un-adapted community, this study investigated responses to NH3 inhibition both at the community-scale and down to individual taxa. The pre-adapted community performed methanogenesis under inhibitory NH3 concentrations better than the un-adapted. While many functionally important phyla were shared between the two communities, only taxa from the pre-adapted community were robust to NH3. Functionally important phyla were mostly comprised of sensitive taxa (≥ 50%), yet all groups, including methanogens, also possessed tolerant individuals (10-50%) suggesting that potential mechanisms for tolerance are non-specific and widespread. Hidden Markov Model-based phylogenetic analysis of methanogens confirmed that NH3 tolerance was not restricted to specific taxonomic groups, even at the genus level. By reconstructing covarying growth patterns via network analyses, methanogenesis by the pre-adapted community was best explained by continued metabolic interactions (edges) between tolerant methanogens and other tolerant taxa (nodes). However, under non-inhibitory conditions, sensitive taxa re-emerged to dominate the pre-adapted community, suggesting that mechanisms of NH3 tolerance can be disadvantageous to fitness without selection pressure. This study demonstrates that methanogenesis under NH3 inhibition depends on broad-scale tolerance throughout the prokaryotic community. Mechanisms for tolerance seem widespread and non-specific, which has practical significance for the development of robust methanogenic biogas communities. KEY POINTS: • Ammonia pre-adaptation allows for better methanogenesis under inhibitory conditions. • All functionally important prokaryote phyla have some ammonia tolerant individuals. • Methanogenesis was likely dependent on interactions between tolerant individuals.

Project description:Ammonia nitrogen is one of the main toxic substances in aquatic cultivation environments. Chronic exposure to excessive amounts of ammonia-N creates toxic consequences, retarding the growth of aquatic organisms. This study investigated the growth performance, morphological and physiological alterations, and transcriptome changes in the hepatopancreas and gills of white shrimp Litopenaeus vannamei. The results showed that there was no significant difference in the survival rate (p > 0.05), whereas growth performance was reduced significantly in the treated groups compared to the control groups (p < 0.05). Significant structural damage and vacuolation occurred in hepatopancreas and gill tissues in the treated groups. Superoxide dismutase (SOD) activity and Na+/K+-ATPase content were significantly increased by chronic ammonia-N exposure in the two tissue groups. In addition, catalase (CAT) activity and malondialdehyde (MDA) levels were significantly altered in the hepatopancreas groups (p < 0.05), whereas no differences were observed in the gill groups (p > 0.05). There were 890 and 1572 differentially expressed genes identified in the hepatopancreas (treated versus control groups) and gills (treated versus control groups), respectively, of L. vannamei under chronic ammonia-N exposure. Functional enrichment analysis revealed associations with oxidative stress, protein synthesis, lipid metabolism, and different serine proteases. The gills maintained cellular homeostasis mainly through high expression of cytoskeleton and transcription genes, whereas the hepatopancreas down-regulated related genes in the ribosome, proteasome, and spliceosome pathways. These genes and pathways are important in the biosynthesis and transformation of living organisms. In addition, both tissues maintained organismal growth primarily through lipid metabolism, which may serve as an effective strategy for ammonia-N resistance in L. vannamei. These results provided a new perspective in understanding the mechanisms of ammonia-N resistance in crustaceans.

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Complex regulatory network allows Myriophyllum aquaticum to thrive under high-concentration ammonia toxicity.

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Complex regulatory network allows Myriophyllum aquaticum to thrive under high-concentration ammonia toxicity.

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