Nejvíce citovaný článek - PubMed ID 19755570
Utricularia carnivory revisited: plants supply photosynthetic carbon to traps
BACKGROUND: Utricularia are rootless aquatic carnivorous plants which have recently attracted the attention of researchers due to the peculiarities of their miniaturized genomes. Here, we focus on a novel aspect of Utricularia ecophysiology-the interactions with and within the complex communities of microorganisms colonizing their traps and external surfaces. RESULTS: Bacteria, fungi, algae, and protozoa inhabit the miniature ecosystem of the Utricularia trap lumen and are involved in the regeneration of nutrients from complex organic matter. By combining molecular methods, microscopy, and other approaches to assess the trap-associated microbial community structure, diversity, function, as well as the nutrient turn-over potential of bacterivory, we gained insight into the nutrient acquisition strategies of the Utricularia hosts. CONCLUSIONS: We conclude that Utricularia traps can, in terms of their ecophysiological function, be compared to microbial cultivators or farms, which center around complex microbial consortia acting synergistically to convert complex organic matter, often of algal origin, into a source of utilizable nutrients for the plants.
- Klíčová slova
- Algae, Bacteria, Ciliate bacterivory, Digestive mutualism, Fungi, Herbivory, Nutrient turnover, Plant–microbe interactions, Protists, Utricularia traps,
- MeSH
- Bacteria klasifikace genetika izolace a purifikace MeSH
- DNA bakterií genetika MeSH
- DNA fungální genetika MeSH
- DNA řas genetika MeSH
- fylogeneze MeSH
- hluchavkotvaré mikrobiologie fyziologie MeSH
- houby klasifikace genetika izolace a purifikace MeSH
- metagenomika metody MeSH
- mikrobiální společenstva MeSH
- stanovení celkové genové exprese metody MeSH
- vodní organismy mikrobiologie fyziologie MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- DNA bakterií MeSH
- DNA fungální MeSH
- DNA řas MeSH
BACKGROUND: The cost-benefit model for the evolution of botanical carnivory provides a conceptual framework for interpreting a wide range of comparative and experimental studies on carnivorous plants. This model assumes that the modified leaves called traps represent a significant cost for the plant, and this cost is outweighed by the benefits from increased nutrient uptake from prey, in terms of enhancing the rate of photosynthesis per unit leaf mass or area (AN) in the microsites inhabited by carnivorous plants. SCOPE: This review summarizes results from the classical interpretation of the cost-benefit model for evolution of botanical carnivory and highlights the costs and benefits of active trapping mechanisms, including water pumping, electrical signalling and accumulation of jasmonates. Novel alternative sequestration strategies (utilization of leaf litter and faeces) in carnivorous plants are also discussed in the context of the cost-benefit model. CONCLUSIONS: Traps of carnivorous plants have lower AN than leaves, and the leaves have higher AN after feeding. Prey digestion, water pumping and electrical signalling represent a significant carbon cost (as an increased rate of respiration, RD) for carnivorous plants. On the other hand, jasmonate accumulation during the digestive period and reprogramming of gene expression from growth and photosynthesis to prey digestion optimizes enzyme production in comparison with constitutive secretion. This inducibility may have evolved as a cost-saving strategy beneficial for carnivorous plants. The similarities between plant defence mechanisms and botanical carnivory are highlighted.
- Klíčová slova
- Action potential, Dionaea, Drosera, Nepenthes, Venus flytrap, botanical carnivory, carnivorous plant, cost–benefit, electrical signalling, jasmonates,
- MeSH
- biologická evoluce * MeSH
- biologické modely * MeSH
- Droseraceae fyziologie MeSH
- fyziologie rostlin * MeSH
- signální transdukce MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- přehledy MeSH
BACKGROUND AND AIMS: Rootless carnivorous plants of the genus Utricularia are important components of many standing waters worldwide, as well as suitable model organisms for studying plant-microbe interactions. In this study, an investigation was made of the importance of microbial dinitrogen (N2) fixation in the N acquisition of four aquatic Utricularia species and another aquatic carnivorous plant, Aldrovanda vesiculosa. METHODS: 16S rRNA amplicon sequencing was used to assess the presence of micro-organisms with known ability to fix N2. Next-generation sequencing provided information on the expression of N2 fixation-associated genes. N2 fixation rates were measured following (15)N2-labelling and were used to calculate the plant assimilation rate of microbially fixed N2. KEY RESULTS: Utricularia traps were confirmed as primary sites of N2 fixation, with up to 16 % of the plant-associated microbial community consisting of bacteria capable of fixing N2. Of these, rhizobia were the most abundant group. Nitrogen fixation rates increased with increasing shoot age, but never exceeded 1·3 μmol N g(-1) d. mass d(-1). Plant assimilation rates of fixed N2 were detectable and significant, but this fraction formed less than 1 % of daily plant N gain. Although trap fluid provides conditions favourable for microbial N2 fixation, levels of nif gene transcription comprised <0·01 % of the total prokaryotic transcripts. CONCLUSIONS: It is hypothesized that the reason for limited N2 fixation in aquatic Utricularia, despite the large potential capacity, is the high concentration of NH4-N (2·0-4·3 mg L(-1)) in the trap fluid. Resulting from fast turnover of organic detritus, it probably inhibits N2 fixation in most of the microorganisms present. Nitrogen fixation is not expected to contribute significantly to N nutrition of aquatic carnivorous plants under their typical growth conditions; however, on an annual basis the plant-microbe system can supply nitrogen in the order of hundreds of mg m(-2) into the nutrient-limited littoral zone, where it may thus represent an important N source.
- Klíčová slova
- 15N2 labelling, Aldrovanda vesiculosa, N nutrition, U. australis, U. intermedia, U. reflexa, Utricularia vulgaris, aquatic carnivorous plants, daily nitrogen gain, nitrogen fixation, periphyton, traps,
- MeSH
- amoniové sloučeniny analýza MeSH
- Bacteria genetika izolace a purifikace metabolismus MeSH
- bakteriální RNA chemie genetika MeSH
- Droseraceae metabolismus mikrobiologie MeSH
- dusík metabolismus MeSH
- ekologie MeSH
- ekosystém MeSH
- fixace dusíku * MeSH
- izotopy dusíku MeSH
- Magnoliopsida metabolismus mikrobiologie MeSH
- molekulární sekvence - údaje MeSH
- RNA ribozomální 16S chemie genetika MeSH
- sekvence nukleotidů MeSH
- sekvenční analýza RNA MeSH
- voda metabolismus MeSH
- výhonky rostlin metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- srovnávací studie MeSH
- Názvy látek
- amoniové sloučeniny MeSH
- bakteriální RNA MeSH
- dusík MeSH
- izotopy dusíku MeSH
- RNA ribozomální 16S MeSH
- voda MeSH
Aquatic Utricularia species usually grow in standing, nutrient-poor humic waters. They take up all necessary nutrients either directly from the water by rootless shoots or from animal prey by traps. The traps are hollow bladders, 1-6 mm long with elastic walls and have a mobile trap door. The inner part of the trap is densely lined with quadrifid and bifid glands and these are involved in the secretion of digestive enzymes, resorption of nutrients and pumping out the water. The traps capture small aquatic animals but they also host a community of microorganisms considered as commensals. How do these perfect traps function, kill and digest their prey? How do they provide ATP energy for their demanding physiological functions? What are the nature of the interactions between the traps and the mutualistic microorganisms living inside as commensals? In this mini review, all of these questions are considered from an ecophysiologist's point of view, based on the most recent literature data and unpublished results. A new concept on the role of the commensal community for the plants is presented.
- MeSH
- ekosystém * MeSH
- kyslík metabolismus MeSH
- Magnoliopsida enzymologie fyziologie MeSH
- potravní řetězec MeSH
- voda fyziologie MeSH
- vodní organismy fyziologie MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- přehledy MeSH
- Názvy látek
- kyslík MeSH
- voda MeSH