skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: De novo Characterization of the Platycladus orientalis Transcriptome and Analysis of Photosynthesis-Related Genes during Aging

Abstract

In China, Platycladus orientalis has a lifespan of thousands of years. The long lifespan of these trees may be relevant for the characterization of plant aging at the molecular level. However, the molecular mechanism of the aging process of P. orientalis is still unknown. To explore the relationship between age and growth of P. orientalis, we analyzed physiological changes during P. orientalis senescence. The malondialdehyde content was greater in 200-, 700-, and 1100-year-old ancient trees than in 20-year-old trees, whereas the peroxidase and superoxide dismutase activities, as well as the soluble protein content, exhibited the opposite trend. Furthermore, we performed a de novo transcriptome assembly using RNA-Seq and obtained 48,044 unigenes with an average length of 896 bp. A total of 418 differentially expressed genes were identified in different stages of aging of P. orientalis. Clustering analysis revealed distinct timepoints at which the oxidation–reduction and photosynthesis pathways changed. Eight clusters with distinct expression patterns were identified. The expression levels of photosynthesis-, oxidation–reduction-, and transporter-related genes were down-regulated, whereas those of transcription-, signaling-, and senescence-related genes were up-regulated during aging. In addition, consistent with the most obviously down-regulated genes of photosynthesis-related genes, the photosynthetic indexes including chlorophyll a and b levelsmore » decreased steadily during P. orientalis aging. This study combined transcriptome with physiological and biochemical data, revealing potential candidate genes influencing senescence during P. orientalis aging.« less

Authors:
 [1]; ORCiD logo [2];  [3];  [4];  [5];  [5];  [5];  [5];  [6]
  1. Chinese Academy of Forestry, Beijing (China). State Key Lab. of Tree Genetics and Breeding, Key Lab. of Tree Breeding and Cultivation of National Forestry and Grassland Administration, Research Inst. of Forestry
  2. Chinese Academy of Forestry, Beijing (China). State Key Lab. of Tree Genetics and Breeding, Key Lab. of Tree Breeding and Cultivation of National Forestry and Grassland Administration, Research Inst. of Forestry; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
  3. Fuyang Normal Univ., Fuyang (China)
  4. Zhongshan Park, Beijing (China)
  5. Chinese Academy of Forestry, Beijing (China). State Key Lab. of Tree Genetics and Breeding, Key Lab. of Tree Breeding and Cultivation of National Forestry and Grassland Administration, Research Inst. of Forestry
  6. Chinese Academy of Forestry, Beijing (China). State Key Lab. of Tree Genetics and Breeding, Key Lab. of Tree Breeding and Cultivation of National Forestry and Grassland Administration, Research Inst. of Forestry, and Research Inst. of Forest Ecology, Environment and Protection
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1511917
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Forests
Additional Journal Information:
Journal Volume: 10; Journal Issue: 5; Journal ID: ISSN 1999-4907
Publisher:
MDPI
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; longevity; Platycladus orientalis; senescence; transcriptome; gene expression

Citation Formats

Chang, Ermei, Zhang, Jin, Yao, Xiamei, Tang, Shuo, Zhao, Xiulian, Deng, Nan, Shi, Shengqing, Liu, Jianfeng, and Jiang, Zeping. De novo Characterization of the Platycladus orientalis Transcriptome and Analysis of Photosynthesis-Related Genes during Aging. United States: N. p., 2019. Web. doi:10.3390/f10050393.
Chang, Ermei, Zhang, Jin, Yao, Xiamei, Tang, Shuo, Zhao, Xiulian, Deng, Nan, Shi, Shengqing, Liu, Jianfeng, & Jiang, Zeping. De novo Characterization of the Platycladus orientalis Transcriptome and Analysis of Photosynthesis-Related Genes during Aging. United States. doi:10.3390/f10050393.
Chang, Ermei, Zhang, Jin, Yao, Xiamei, Tang, Shuo, Zhao, Xiulian, Deng, Nan, Shi, Shengqing, Liu, Jianfeng, and Jiang, Zeping. Fri . "De novo Characterization of the Platycladus orientalis Transcriptome and Analysis of Photosynthesis-Related Genes during Aging". United States. doi:10.3390/f10050393. https://www.osti.gov/servlets/purl/1511917.
@article{osti_1511917,
title = {De novo Characterization of the Platycladus orientalis Transcriptome and Analysis of Photosynthesis-Related Genes during Aging},
author = {Chang, Ermei and Zhang, Jin and Yao, Xiamei and Tang, Shuo and Zhao, Xiulian and Deng, Nan and Shi, Shengqing and Liu, Jianfeng and Jiang, Zeping},
abstractNote = {In China, Platycladus orientalis has a lifespan of thousands of years. The long lifespan of these trees may be relevant for the characterization of plant aging at the molecular level. However, the molecular mechanism of the aging process of P. orientalis is still unknown. To explore the relationship between age and growth of P. orientalis, we analyzed physiological changes during P. orientalis senescence. The malondialdehyde content was greater in 200-, 700-, and 1100-year-old ancient trees than in 20-year-old trees, whereas the peroxidase and superoxide dismutase activities, as well as the soluble protein content, exhibited the opposite trend. Furthermore, we performed a de novo transcriptome assembly using RNA-Seq and obtained 48,044 unigenes with an average length of 896 bp. A total of 418 differentially expressed genes were identified in different stages of aging of P. orientalis. Clustering analysis revealed distinct timepoints at which the oxidation–reduction and photosynthesis pathways changed. Eight clusters with distinct expression patterns were identified. The expression levels of photosynthesis-, oxidation–reduction-, and transporter-related genes were down-regulated, whereas those of transcription-, signaling-, and senescence-related genes were up-regulated during aging. In addition, consistent with the most obviously down-regulated genes of photosynthesis-related genes, the photosynthetic indexes including chlorophyll a and b levels decreased steadily during P. orientalis aging. This study combined transcriptome with physiological and biochemical data, revealing potential candidate genes influencing senescence during P. orientalis aging.},
doi = {10.3390/f10050393},
journal = {Forests},
number = 5,
volume = 10,
place = {United States},
year = {2019},
month = {5}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Save / Share:

Works referenced in this record:

Aging in Perennials
journal, June 2007


Transcriptome differences between 20- and 3,000-year-old Platycladus orientalis reveal that ROS are involved in senescence regulation
journal, September 2017


Physiology and proteomics research on the leaves of ancient Platycladus orientalis (L.) during winter
journal, August 2015


Ageing and the mystery at Arles
journal, May 2004

  • Nemoto, Shino; Finkel, Toren
  • Nature, Vol. 429, Issue 6988
  • DOI: 10.1038/429149a

Senescence, ageing and death of the whole plant: morphological prerequisites and constraints of plant immortality
journal, November 2014

  • Klimešová, Jitka; Nobis, Michael Peter; Herben, Tomáš
  • New Phytologist, Vol. 206, Issue 1
  • DOI: 10.1111/nph.13160

How do tree structure and old age affect growth potential of California redwoods?
journal, May 2015

  • Sillett, Stephen C.; Van Pelt, Robert; Carroll, Allyson L.
  • Ecological Monographs, Vol. 85, Issue 2
  • DOI: 10.1890/14-1016.1

Do perennials really senesce?
journal, May 2008


Senescence-Related Changes in the Leaf Apoplast
journal, November 2013


A big issue for trees
journal, October 2005


Extreme longevity in trees: live slow, die old?
journal, October 2010


NADPH oxidases differentially regulate ROS metabolism and nutrient uptake under cadmium toxicity
journal, January 2016

  • Gupta, D. K.; Pena, L. B.; Romero‐Puertas, M. C.
  • Plant, Cell & Environment, Vol. 40, Issue 4
  • DOI: 10.1111/pce.12711

Functional Analysis of the Arabidopsis PAL Gene Family in Plant Growth, Development, and Response to Environmental Stress
journal, June 2010


A Cellular Timetable of Autumn Senescence
journal, November 2005

  • Keskitalo, Johanna; Bergquist, Gustaf; Gardeström, Per
  • Plant Physiology, Vol. 139, Issue 4
  • DOI: 10.1104/pp.105.066845

Plant aging increases oxidative stress in chloroplasts
journal, February 2002


Plant age-related changes in cytokinins, leaf growth and pigment accumulation in juvenile mastic trees
journal, March 2013


Photosynthetic capacity of senescent leaves for a subtropical broadleaf deciduous tree species Liquidambar formosana Hance
journal, July 2017


Universal scaling of respiratory metabolism, size and nitrogen in plants
journal, January 2006

  • Reich, Peter B.; Tjoelker, Mark G.; Machado, Jose-Luis
  • Nature, Vol. 439, Issue 7075
  • DOI: 10.1038/nature04282

Transcriptome of Arabidopsis leaf senescence
journal, May 2004


Identification and characterization of nuclear genes involved in photosynthesis in Populus
journal, January 2014


Gene Expression in Autumn Leaves
journal, January 2003

  • Bhalerao, Rupali; Keskitalo, Johanna; Sterky, Fredrik
  • Plant Physiology, Vol. 131, Issue 2
  • DOI: 10.1104/pp.012732

Photoperoxidation in isolated chloroplasts
journal, April 1968


Leaf Senescence: Correlated with Increased Levels of Membrane Permeability and Lipid Peroxidation, and Decreased Levels of Superoxide Dismutase and Catalase
journal, January 1981

  • Dhindsa, Rajinder S.; Plumb-Dhindsa, Pamela; Thorpe, Trevor A.
  • Journal of Experimental Botany, Vol. 32, Issue 1
  • DOI: 10.1093/jxb/32.1.93

High-Resolution Temporal Profiling of Transcripts during Arabidopsis Leaf Senescence Reveals a Distinct Chronology of Processes and Regulation
journal, March 2011

  • Breeze, Emily; Harrison, Elizabeth; McHattie, Stuart
  • The Plant Cell, Vol. 23, Issue 3
  • DOI: 10.1105/tpc.111.083345

Full-length transcriptome assembly from RNA-Seq data without a reference genome
journal, May 2011

  • Grabherr, Manfred G.; Haas, Brian J.; Yassour, Moran
  • Nature Biotechnology, Vol. 29, Issue 7
  • DOI: 10.1038/nbt.1883

Mapping and quantifying mammalian transcriptomes by RNA-Seq
journal, May 2008

  • Mortazavi, Ali; Williams, Brian A.; McCue, Kenneth
  • Nature Methods, Vol. 5, Issue 7, p. 621-628
  • DOI: 10.1038/nmeth.1226

Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research
journal, August 2005


Differences in gene expression between natural and artificially induced leaf senescence in barley
journal, March 2015


Long-term exogenous application of melatonin delays drought-induced leaf senescence in apple
journal, October 2012

  • Wang, Ping; Sun, Xun; Li, Chao
  • Journal of Pineal Research, Vol. 54, Issue 3
  • DOI: 10.1111/jpi.12017

Structure Determination and Improved Model of Plant Photosystem I
journal, November 2009

  • Amunts, Alexey; Toporik, Hila; Borovikova, Anna
  • Journal of Biological Chemistry, Vol. 285, Issue 5
  • DOI: 10.1074/jbc.M109.072645

Stomatal conductance and photosynthesis vary linearly with plant hydraulic conductance in ponderosa pine
journal, January 2001


Reactive oxygen species and nitric oxide in plant mitochondria: origin and redundant regulatory systems
journal, April 2010


Changes in carotenoids and ABA content in Citrus leaves in response to girdling
journal, February 2011


Two-dimensional zymography in detection of proteolytic enzymes in wheat leaves
journal, September 2013

  • Grudkowska, Małgorzata; Lisik, Piotr; Rybka, Krystyna
  • Acta Physiologiae Plantarum, Vol. 35, Issue 12
  • DOI: 10.1007/s11738-013-1371-1

Silencing of mitochondrial uncoupling protein gene aggravates chilling stress by altering mitochondrial respiration and electron transport in tomato
journal, October 2015

  • Liu, Airong; Chen, Shuangchen; Wang, Mengmeng
  • Acta Physiologiae Plantarum, Vol. 37, Issue 11
  • DOI: 10.1007/s11738-015-1974-9

Mitochondria, oxidative stress and cell death
journal, February 2007


ω-Hydroxylation of epoxy- and hydroxy-fatty acids by CYP94AI: possible involvement in plant defence
journal, December 2000

  • Pinot, F.; Skrabs, M.; Compagnon, V.
  • Biochemical Society Transactions, Vol. 28, Issue 6
  • DOI: 10.1042/bst0280867

Analysis of Telomere Length and Telomerase Activity in Tree Species of Various Lifespans, and with Age in the Bristlecone Pine Pinus longaeva
journal, March 2006

  • Flanary, Barry E.; Kletetschka, Gunther
  • Rejuvenation Research, Vol. 9, Issue 1
  • DOI: 10.1089/rej.2006.9.61

    Works referencing / citing this record:

    Photosynthetic capacity of senescent leaves for a subtropical broadleaf deciduous tree species Liquidambar formosana Hance
    journal, July 2017


    Transcriptome of Arabidopsis leaf senescence
    journal, May 2004


    Do perennials really senesce?
    journal, May 2008


    Photoperoxidation in isolated chloroplasts
    journal, April 1968


    Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research
    journal, August 2005


    Extreme longevity in trees: live slow, die old?
    journal, October 2010


    A big issue for trees
    journal, October 2005


    Long-term exogenous application of melatonin delays drought-induced leaf senescence in apple
    journal, October 2012

    • Wang, Ping; Sun, Xun; Li, Chao
    • Journal of Pineal Research, Vol. 54, Issue 3
    • DOI: 10.1111/jpi.12017

    Ageing and the mystery at Arles
    journal, May 2004

    • Nemoto, Shino; Finkel, Toren
    • Nature, Vol. 429, Issue 6988
    • DOI: 10.1038/429149a

    Transcriptome differences between 20- and 3,000-year-old Platycladus orientalis reveal that ROS are involved in senescence regulation
    journal, September 2017


    Senescence-Related Changes in the Leaf Apoplast
    journal, November 2013


    Silencing of mitochondrial uncoupling protein gene aggravates chilling stress by altering mitochondrial respiration and electron transport in tomato
    journal, October 2015

    • Liu, Airong; Chen, Shuangchen; Wang, Mengmeng
    • Acta Physiologiae Plantarum, Vol. 37, Issue 11
    • DOI: 10.1007/s11738-015-1974-9

    A Cellular Timetable of Autumn Senescence
    journal, November 2005

    • Keskitalo, Johanna; Bergquist, Gustaf; Gardeström, Per
    • Plant Physiology, Vol. 139, Issue 4
    • DOI: 10.1104/pp.105.066845

    Identification and characterization of nuclear genes involved in photosynthesis in Populus
    journal, January 2014


    Functional Analysis of the Arabidopsis PAL Gene Family in Plant Growth, Development, and Response to Environmental Stress
    journal, June 2010


    Physiology and proteomics research on the leaves of ancient Platycladus orientalis (L.) during winter
    journal, August 2015


    Mitochondria, oxidative stress and cell death
    journal, February 2007


    ω-Hydroxylation of epoxy- and hydroxy-fatty acids by CYP94AI: possible involvement in plant defence
    journal, December 2000

    • Pinot, F.; Skrabs, M.; Compagnon, V.
    • Biochemical Society Transactions, Vol. 28, Issue 6
    • DOI: 10.1042/bst0280867

    How do tree structure and old age affect growth potential of California redwoods?
    journal, May 2015

    • Sillett, Stephen C.; Van Pelt, Robert; Carroll, Allyson L.
    • Ecological Monographs, Vol. 85, Issue 2
    • DOI: 10.1890/14-1016.1

    Changes in carotenoids and ABA content in Citrus leaves in response to girdling
    journal, February 2011


    High-Resolution Temporal Profiling of Transcripts during Arabidopsis Leaf Senescence Reveals a Distinct Chronology of Processes and Regulation
    journal, March 2011

    • Breeze, Emily; Harrison, Elizabeth; McHattie, Stuart
    • The Plant Cell, Vol. 23, Issue 3
    • DOI: 10.1105/tpc.111.083345

    Senescence, ageing and death of the whole plant: morphological prerequisites and constraints of plant immortality
    journal, November 2014

    • Klimešová, Jitka; Nobis, Michael Peter; Herben, Tomáš
    • New Phytologist, Vol. 206, Issue 1
    • DOI: 10.1111/nph.13160

    NADPH oxidases differentially regulate ROS metabolism and nutrient uptake under cadmium toxicity
    journal, January 2016

    • Gupta, D. K.; Pena, L. B.; Romero‐Puertas, M. C.
    • Plant, Cell & Environment, Vol. 40, Issue 4
    • DOI: 10.1111/pce.12711

    Does bristlecone pine senesce?
    journal, April 2001


    Plant age-related changes in cytokinins, leaf growth and pigment accumulation in juvenile mastic trees
    journal, March 2013


    Universal scaling of respiratory metabolism, size and nitrogen in plants
    journal, January 2006

    • Reich, Peter B.; Tjoelker, Mark G.; Machado, Jose-Luis
    • Nature, Vol. 439, Issue 7075
    • DOI: 10.1038/nature04282

    Gene Expression in Autumn Leaves
    journal, January 2003

    • Bhalerao, Rupali; Keskitalo, Johanna; Sterky, Fredrik
    • Plant Physiology, Vol. 131, Issue 2
    • DOI: 10.1104/pp.012732

    Mapping and quantifying mammalian transcriptomes by RNA-Seq
    journal, May 2008

    • Mortazavi, Ali; Williams, Brian A.; McCue, Kenneth
    • Nature Methods, Vol. 5, Issue 7, p. 621-628
    • DOI: 10.1038/nmeth.1226

    Stomatal conductance and photosynthesis vary linearly with plant hydraulic conductance in ponderosa pine
    journal, January 2001


    Plant aging increases oxidative stress in chloroplasts
    journal, February 2002


    Reactive oxygen species and nitric oxide in plant mitochondria: origin and redundant regulatory systems
    journal, April 2010


    Two-dimensional zymography in detection of proteolytic enzymes in wheat leaves
    journal, September 2013

    • Grudkowska, Małgorzata; Lisik, Piotr; Rybka, Krystyna
    • Acta Physiologiae Plantarum, Vol. 35, Issue 12
    • DOI: 10.1007/s11738-013-1371-1

    Full-length transcriptome assembly from RNA-Seq data without a reference genome
    journal, May 2011

    • Grabherr, Manfred G.; Haas, Brian J.; Yassour, Moran
    • Nature Biotechnology, Vol. 29, Issue 7
    • DOI: 10.1038/nbt.1883

    Aging in Perennials
    journal, June 2007


    Differences in gene expression between natural and artificially induced leaf senescence in barley
    journal, March 2015


    Leaf Senescence: Correlated with Increased Levels of Membrane Permeability and Lipid Peroxidation, and Decreased Levels of Superoxide Dismutase and Catalase
    journal, January 1981

    • Dhindsa, Rajinder S.; Plumb-Dhindsa, Pamela; Thorpe, Trevor A.
    • Journal of Experimental Botany, Vol. 32, Issue 1
    • DOI: 10.1093/jxb/32.1.93