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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...

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Autores principales: 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
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2020
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.
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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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