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Light-responsive expression atlas reveals the effects of light quality and intensity in Kalanchoë fedtschenkoi, a plant with crassulacean acid metabolism
BACKGROUND: Crassulacean acid metabolism (CAM), a specialized mode of photosynthesis, enables plant adaptation to water-limited environments and improves photosynthetic efficiency via an inorganic carbon-concentrating mechanism. Kalanchoë fedtschenkoi is an obligate CAM model featuring a relatively...
Autores principales: | , , , , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Oxford University Press
2020
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7058158/ https://www.ncbi.nlm.nih.gov/pubmed/32135007 http://dx.doi.org/10.1093/gigascience/giaa018 |
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author | Zhang, Jin Hu, Rongbin Sreedasyam, Avinash Garcia, Travis M Lipzen, Anna Wang, Mei Yerramsetty, Pradeep Liu, Degao Ng, Vivian Schmutz, Jeremy Cushman, John C Borland, Anne M Pasha, Asher Provart, Nicholas J Chen, Jin-Gui Muchero, Wellington Tuskan, Gerald A Yang, Xiaohan |
author_facet | Zhang, Jin Hu, Rongbin Sreedasyam, Avinash Garcia, Travis M Lipzen, Anna Wang, Mei Yerramsetty, Pradeep Liu, Degao Ng, Vivian Schmutz, Jeremy Cushman, John C Borland, Anne M Pasha, Asher Provart, Nicholas J Chen, Jin-Gui Muchero, Wellington Tuskan, Gerald A Yang, Xiaohan |
author_sort | Zhang, Jin |
collection | PubMed |
description | BACKGROUND: Crassulacean acid metabolism (CAM), a specialized mode of photosynthesis, enables plant adaptation to water-limited environments and improves photosynthetic efficiency via an inorganic carbon-concentrating mechanism. Kalanchoë fedtschenkoi is an obligate CAM model featuring a relatively small genome and easy stable transformation. However, the molecular responses to light quality and intensity in CAM plants remain understudied. RESULTS: Here we present a genome-wide expression atlas of K. fedtschenkoi plants grown under 12 h/12 h photoperiod with different light quality (blue, red, far-red, white light) and intensity (0, 150, 440, and 1,000 μmol m(–2) s(–1)) based on RNA sequencing performed for mature leaf samples collected at dawn (2 h before the light period) and dusk (2 h before the dark period). An eFP web browser was created for easy access of the gene expression data. Based on the expression atlas, we constructed a light-responsive co-expression network to reveal the potential regulatory relationships in K. fedtschenkoi. Measurements of leaf titratable acidity, soluble sugar, and starch turnover provided metabolic indicators of the magnitude of CAM under the different light treatments and were used to provide biological context for the expression dataset. Furthermore, CAM-related subnetworks were highlighted to showcase genes relevant to CAM pathway, circadian clock, and stomatal movement. In comparison with white light, monochrome blue/red/far-red light treatments repressed the expression of several CAM-related genes at dusk, along with a major reduction in acid accumulation. Increasing light intensity from an intermediate level (440 μmol m(−2) s(−1)) of white light to a high light treatment (1,000 μmol m(–2) s(–1)) increased expression of several genes involved in dark CO(2) fixation and malate transport at dawn, along with an increase in organic acid accumulation. CONCLUSIONS: This study provides a useful genomics resource for investigating the molecular mechanism underlying the light regulation of physiology and metabolism in CAM plants. Our results support the hypothesis that both light intensity and light quality can modulate the CAM pathway through regulation of CAM-related genes in K. fedtschenkoi. |
format | Online Article Text |
id | pubmed-7058158 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2020 |
publisher | Oxford University Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-70581582020-03-13 Light-responsive expression atlas reveals the effects of light quality and intensity in Kalanchoë fedtschenkoi, a plant with crassulacean acid metabolism Zhang, Jin Hu, Rongbin Sreedasyam, Avinash Garcia, Travis M Lipzen, Anna Wang, Mei Yerramsetty, Pradeep Liu, Degao Ng, Vivian Schmutz, Jeremy Cushman, John C Borland, Anne M Pasha, Asher Provart, Nicholas J Chen, Jin-Gui Muchero, Wellington Tuskan, Gerald A Yang, Xiaohan Gigascience Data Note BACKGROUND: Crassulacean acid metabolism (CAM), a specialized mode of photosynthesis, enables plant adaptation to water-limited environments and improves photosynthetic efficiency via an inorganic carbon-concentrating mechanism. Kalanchoë fedtschenkoi is an obligate CAM model featuring a relatively small genome and easy stable transformation. However, the molecular responses to light quality and intensity in CAM plants remain understudied. RESULTS: Here we present a genome-wide expression atlas of K. fedtschenkoi plants grown under 12 h/12 h photoperiod with different light quality (blue, red, far-red, white light) and intensity (0, 150, 440, and 1,000 μmol m(–2) s(–1)) based on RNA sequencing performed for mature leaf samples collected at dawn (2 h before the light period) and dusk (2 h before the dark period). An eFP web browser was created for easy access of the gene expression data. Based on the expression atlas, we constructed a light-responsive co-expression network to reveal the potential regulatory relationships in K. fedtschenkoi. Measurements of leaf titratable acidity, soluble sugar, and starch turnover provided metabolic indicators of the magnitude of CAM under the different light treatments and were used to provide biological context for the expression dataset. Furthermore, CAM-related subnetworks were highlighted to showcase genes relevant to CAM pathway, circadian clock, and stomatal movement. In comparison with white light, monochrome blue/red/far-red light treatments repressed the expression of several CAM-related genes at dusk, along with a major reduction in acid accumulation. Increasing light intensity from an intermediate level (440 μmol m(−2) s(−1)) of white light to a high light treatment (1,000 μmol m(–2) s(–1)) increased expression of several genes involved in dark CO(2) fixation and malate transport at dawn, along with an increase in organic acid accumulation. CONCLUSIONS: This study provides a useful genomics resource for investigating the molecular mechanism underlying the light regulation of physiology and metabolism in CAM plants. Our results support the hypothesis that both light intensity and light quality can modulate the CAM pathway through regulation of CAM-related genes in K. fedtschenkoi. Oxford University Press 2020-03-05 /pmc/articles/PMC7058158/ /pubmed/32135007 http://dx.doi.org/10.1093/gigascience/giaa018 Text en © The Author(s) 2020. Published by Oxford University Press. http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. |
spellingShingle | Data Note Zhang, Jin Hu, Rongbin Sreedasyam, Avinash Garcia, Travis M Lipzen, Anna Wang, Mei Yerramsetty, Pradeep Liu, Degao Ng, Vivian Schmutz, Jeremy Cushman, John C Borland, Anne M Pasha, Asher Provart, Nicholas J Chen, Jin-Gui Muchero, Wellington Tuskan, Gerald A Yang, Xiaohan Light-responsive expression atlas reveals the effects of light quality and intensity in Kalanchoë fedtschenkoi, a plant with crassulacean acid metabolism |
title | Light-responsive expression atlas reveals the effects of light quality and intensity in Kalanchoë fedtschenkoi, a plant with crassulacean acid metabolism |
title_full | Light-responsive expression atlas reveals the effects of light quality and intensity in Kalanchoë fedtschenkoi, a plant with crassulacean acid metabolism |
title_fullStr | Light-responsive expression atlas reveals the effects of light quality and intensity in Kalanchoë fedtschenkoi, a plant with crassulacean acid metabolism |
title_full_unstemmed | Light-responsive expression atlas reveals the effects of light quality and intensity in Kalanchoë fedtschenkoi, a plant with crassulacean acid metabolism |
title_short | Light-responsive expression atlas reveals the effects of light quality and intensity in Kalanchoë fedtschenkoi, a plant with crassulacean acid metabolism |
title_sort | light-responsive expression atlas reveals the effects of light quality and intensity in kalanchoë fedtschenkoi, a plant with crassulacean acid metabolism |
topic | Data Note |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7058158/ https://www.ncbi.nlm.nih.gov/pubmed/32135007 http://dx.doi.org/10.1093/gigascience/giaa018 |
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