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Plant sphingolipids: Their importance in cellular organization and adaption.

ABSTRACT: Sphingolipids and their phosphorylated derivatives are ubiquitous bio-active components of cells. They are structural elements in the lipid bilayer and contribute to the dynamic nature of the membrane. They have been implicated in many cellular processes in yeast and animal cells, including aspects of signaling, apoptosis, and senescence. Although sphingolipids have a better defined role in animal systems, they have been shown to be central to many essential processes in plants including but not limited to, pollen development, signal transduction and in the response to biotic and abiotic stress. A fuller understanding of the roles of sphingolipids within plants has been facilitated by classical biochemical studies and the identification of mutants of model species. Recently the development of powerful mass spectrometry techniques hailed the advent of the emerging field of lipidomics enabling more accurate sphingolipid detection and quantitation. This review will consider plant sphingolipid biosynthesis and function in the context of these new developments. This article is part of a Special Issue entitled: Plant Lipid Biology edited by Kent D. Chapman and Ivo Feussner.

SUBMITTER: Michaelson LV

PROVIDER: S-EPMC4970446 | biostudies-literature | 2016 Sep

REPOSITORIES: biostudies-literature

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Plant sphingolipids: Their importance in cellular organization and adaption.

Michaelson Louise V LV Napier Johnathan A JA Molino Diana D Faure Jean-Denis JD

Biochimica et biophysica acta 20160413 9 Pt B

Sphingolipids and their phosphorylated derivatives are ubiquitous bio-active components of cells. They are structural elements in the lipid bilayer and contribute to the dynamic nature of the membrane. They have been implicated in many cellular processes in yeast and animal cells, including aspects of signaling, apoptosis, and senescence. Although sphingolipids have a better defined role in animal systems, they have been shown to be central to many essential processes in plants including but not ...[more]

PMID: 27086144

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Project description:Fungi dominate the recycling of carbon sequestered in woody biomass. This process of organic turnover was first evolved among "white rot" fungi that degrade lignin to access carbohydrates and later evolved multiple times toward more efficient strategies to selectively target carbohydrates-"brown rot." The brown rot adaption was often explained by mechanisms to deploy reactive oxygen species (ROS) to oxidatively attack wood structures. However, its genetic basis remains unclear, especially in the context of gene contractions of conventional carbohydrate-active enzymes (CAZYs) relative to white rot ancestors. Here, we hypothesized that these apparent gains in brown rot efficiency despite gene losses were due, in part, to upregulation of the retained genes. We applied comparative transcriptomics to multiple species of both rot types grown across a wood wafer to create a gradient of progressive decay and to enable tracking temporal gene expression. Dozens of "decay-stage-dependent" ortho-genes were isolated, narrowing a pool of candidate genes with time-dependent regulation unique to brown rot fungi. A broad comparison of the expression timing of CAZY families indicated a temporal regulatory shift of lignocellulose-oxidizing genes toward early stages in brown rot compared to white rot, enabling the segregation of oxidative treatment ahead of hydrolysis. These key brown rot ROS-generating genes with iron ion binding functions were isolated. Moreover, transcription energy was shifted to be invested on the retained GHs in brown rot fungi to strengthen carbohydrate conversion. Collectively, these results support the hypothesis that gene regulation shifts played a pivotal role in brown rot adaptation.IMPORTANCE Fungi dominate the turnover of wood, Earth's largest pool of aboveground terrestrial carbon. Fungi first evolved this capacity by degrading lignin to access and hydrolyze embedded carbohydrates (white rot). Multiple lineages, however, adapted faster reactive oxygen species (ROS) pretreatments to loosen lignocellulose and selectively extract sugars (brown rot). This brown rot "shortcut" often coincided with losses (>60%) of conventional lignocellulolytic genes, implying that ROS adaptations supplanted conventional pathways. We used comparative transcriptomics to further pursue brown rot adaptations, which illuminated the clear temporal expression shift of ROS genes, as well as the shift toward synthesizing more GHs in brown rot relative to white rot. These imply that gene regulatory shifts, not simply ROS innovations, were key to brown rot fungal evolution. These results not only reveal an important biological shift among these unique fungi, but they may also illuminate a trait that restricts brown rot fungi to certain ecological niches.

Project description:BackgroundVegetation succession is one of the major driving processes of grassland degradation. Stoichiometry significantly contributes to vegetation dynamics. However, a knowledge gap exists in how soil nutrients and root enzymes influence the stoichiometric ratio to affect vegetation dynamics.MethodsTo address these questions, we selected a dominant species (Leymus chinensis (Trin.) Tzvel.) and a degraded-dominant species (Artemisia frigida Willd.) under different management regimes (enclosure and grazing) on the Inner Mongolia steppe. We measured (i) plant nutrient concentrations, (ii) root enzymes and (iii) soil nutrients to investigate how the selected plant species responded to grazing.ResultsThe results show that: (i) N and P concentrations and the C:N:P ratio in different organs are significantly affected by grazing, and there is variation in the plant species' response. Grazing significantly increased N and P in the leaves and stems of L. chinensis and the stems and roots of A. frigida. (ii) Grazing significantly increased the activities of glutamine synthase but decreased the activities of acid phosphatase in L. chinensis. The nitrate reductase and acid phosphatase activities significantly increased in A. frigida under grazing conditions. (iii) Grazing decreased the total nitrogen, total phosphorus, and available nitrogen, but increased the available phosphorus in the soil.ConclusionWe conclude that A. frigida is better adapted to grazing than L. chinensis, possibly because of its relatively increased stem and root growth, which enhance population expansion following grazing. Conversely, L. chinensis showed increased leaf and stem growth, but suffered nutrient and biomass loss as a result of excessive foraging by livestock, which severely affected its ability to colonize. Root enzymes coupled with soil nutrients can regulate plant nutrients and stoichiometric ratios as an adaptive response to grazing. Thus, we demonstrated that stoichiometric ratios allow species to better withstand grazing disturbances. This study provides a new understanding of the mechanisms involved in grazing-resistance within a plant-soil system.

Dataset Information

Plant sphingolipids: Their importance in cellular organization and adaption.

Publications

Plant sphingolipids: Their importance in cellular organization and adaption.

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