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Cytochrome c levels affect the TOR pathway to regulate growth and metabolism under energy‐deficient conditions
Summary Mitochondrial function is essential for plant growth, but the mechanisms involved in adjusting growth and metabolism to changes in mitochondrial energy production are not fully understood. We studied plants with reduced expression of CYTC‐1, one of two genes encoding the respiratory chain co...
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| Published in: | The New phytologist 2024-03, Vol.241 (5), p.2039-2058 |
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| Main Authors: | , , , , , , |
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| container_end_page | 2058 |
| container_issue | 5 |
| container_start_page | 2039 |
| container_title | The New phytologist |
| container_volume | 241 |
| creator | Canal, María Victoria Mansilla, Natanael Gras, Diana E. Ibarra, Agustín Figueroa, Carlos M. Gonzalez, Daniel H. Welchen, Elina |
| description | Summary
Mitochondrial function is essential for plant growth, but the mechanisms involved in adjusting growth and metabolism to changes in mitochondrial energy production are not fully understood.
We studied plants with reduced expression of CYTC‐1, one of two genes encoding the respiratory chain component cytochrome c (CYTc) in Arabidopsis, to understand how mitochondria communicate their status to coordinate metabolism and growth.
Plants with CYTc deficiency show decreased mitochondrial membrane potential and lower ATP content, even when carbon sources are present. They also exhibit higher free amino acid content, induced autophagy, and increased resistance to nutritional stress caused by prolonged darkness, similar to plants with triggered starvation signals. CYTc deficiency affects target of rapamycin (TOR)‐pathway activation, reducing S6 kinase (S6K) and RPS6A phosphorylation, as well as total S6K protein levels due to increased protein degradation via proteasome and autophagy. TOR overexpression restores growth and other parameters affected in cytc‐1 mutants, even if mitochondrial membrane potential and ATP levels remain low.
We propose that CYTc‐deficient plants coordinate their metabolism and energy availability by reducing TOR‐pathway activation as a preventive signal to adjust growth in anticipation of energy exhaustion, thus providing a mechanism by which changes in mitochondrial activity are transduced to the rest of the cell. |
| doi_str_mv | 10.1111/nph.19506 |
| format | article |
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Mitochondrial function is essential for plant growth, but the mechanisms involved in adjusting growth and metabolism to changes in mitochondrial energy production are not fully understood.
We studied plants with reduced expression of CYTC‐1, one of two genes encoding the respiratory chain component cytochrome c (CYTc) in Arabidopsis, to understand how mitochondria communicate their status to coordinate metabolism and growth.
Plants with CYTc deficiency show decreased mitochondrial membrane potential and lower ATP content, even when carbon sources are present. They also exhibit higher free amino acid content, induced autophagy, and increased resistance to nutritional stress caused by prolonged darkness, similar to plants with triggered starvation signals. CYTc deficiency affects target of rapamycin (TOR)‐pathway activation, reducing S6 kinase (S6K) and RPS6A phosphorylation, as well as total S6K protein levels due to increased protein degradation via proteasome and autophagy. TOR overexpression restores growth and other parameters affected in cytc‐1 mutants, even if mitochondrial membrane potential and ATP levels remain low.
We propose that CYTc‐deficient plants coordinate their metabolism and energy availability by reducing TOR‐pathway activation as a preventive signal to adjust growth in anticipation of energy exhaustion, thus providing a mechanism by which changes in mitochondrial activity are transduced to the rest of the cell.</description><identifier>ISSN: 0028-646X</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.19506</identifier><identifier>PMID: 38191763</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Adenosine Triphosphate - metabolism ; Amino acids ; Arabidopsis - metabolism ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Arabidopsis thaliana ; ATP ; Autophagy ; Biodegradation ; Carbon sources ; Cytochrome ; Cytochrome c ; Cytochromes ; Cytochromes c - genetics ; Cytochromes c - metabolism ; Darkness ; Electron transport ; Energy ; energy deficiency ; Energy metabolism ; Genes ; Kinases ; Membrane potential ; Membranes ; Metabolism ; Mitochondria ; Nutrient deficiency ; Phosphatidylinositol 3-Kinases - metabolism ; Phosphorylation ; Plant growth ; Plants ; Proteasomes ; Proteins ; Rapamycin ; Ribosomal Protein S6 Kinases - metabolism ; Sirolimus - pharmacology ; starvation ; target of rapamycin ; TOR protein</subject><ispartof>The New phytologist, 2024-03, Vol.241 (5), p.2039-2058</ispartof><rights>2024 The Authors. © 2024 New Phytologist Foundation</rights><rights>2024 The Authors. New Phytologist © 2024 New Phytologist Foundation.</rights><rights>Copyright © 2024 New Phytologist Trust</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c3136-c4a74e458df4a416300c11b85d7689e75f2a615aaac7d20700979595cffbfa643</cites><orcidid>0009-0003-7726-395X ; 0000-0001-6052-3223 ; 0000-0003-4025-573X ; 0000-0003-4047-0480 ; 0000-0002-3137-8095 ; 0009-0000-0874-1995 ; 0009-0000-0690-6813</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fnph.19506$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fnph.19506$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>315,786,790,27957,27958,50923,51032</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38191763$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Canal, María Victoria</creatorcontrib><creatorcontrib>Mansilla, Natanael</creatorcontrib><creatorcontrib>Gras, Diana E.</creatorcontrib><creatorcontrib>Ibarra, Agustín</creatorcontrib><creatorcontrib>Figueroa, Carlos M.</creatorcontrib><creatorcontrib>Gonzalez, Daniel H.</creatorcontrib><creatorcontrib>Welchen, Elina</creatorcontrib><title>Cytochrome c levels affect the TOR pathway to regulate growth and metabolism under energy‐deficient conditions</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>Summary
Mitochondrial function is essential for plant growth, but the mechanisms involved in adjusting growth and metabolism to changes in mitochondrial energy production are not fully understood.
We studied plants with reduced expression of CYTC‐1, one of two genes encoding the respiratory chain component cytochrome c (CYTc) in Arabidopsis, to understand how mitochondria communicate their status to coordinate metabolism and growth.
Plants with CYTc deficiency show decreased mitochondrial membrane potential and lower ATP content, even when carbon sources are present. They also exhibit higher free amino acid content, induced autophagy, and increased resistance to nutritional stress caused by prolonged darkness, similar to plants with triggered starvation signals. CYTc deficiency affects target of rapamycin (TOR)‐pathway activation, reducing S6 kinase (S6K) and RPS6A phosphorylation, as well as total S6K protein levels due to increased protein degradation via proteasome and autophagy. TOR overexpression restores growth and other parameters affected in cytc‐1 mutants, even if mitochondrial membrane potential and ATP levels remain low.
We propose that CYTc‐deficient plants coordinate their metabolism and energy availability by reducing TOR‐pathway activation as a preventive signal to adjust growth in anticipation of energy exhaustion, thus providing a mechanism by which changes in mitochondrial activity are transduced to the rest of the cell.</description><subject>Adenosine Triphosphate - metabolism</subject><subject>Amino acids</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Arabidopsis thaliana</subject><subject>ATP</subject><subject>Autophagy</subject><subject>Biodegradation</subject><subject>Carbon sources</subject><subject>Cytochrome</subject><subject>Cytochrome c</subject><subject>Cytochromes</subject><subject>Cytochromes c - genetics</subject><subject>Cytochromes c - metabolism</subject><subject>Darkness</subject><subject>Electron transport</subject><subject>Energy</subject><subject>energy deficiency</subject><subject>Energy metabolism</subject><subject>Genes</subject><subject>Kinases</subject><subject>Membrane potential</subject><subject>Membranes</subject><subject>Metabolism</subject><subject>Mitochondria</subject><subject>Nutrient deficiency</subject><subject>Phosphatidylinositol 3-Kinases - metabolism</subject><subject>Phosphorylation</subject><subject>Plant growth</subject><subject>Plants</subject><subject>Proteasomes</subject><subject>Proteins</subject><subject>Rapamycin</subject><subject>Ribosomal Protein S6 Kinases - metabolism</subject><subject>Sirolimus - pharmacology</subject><subject>starvation</subject><subject>target of rapamycin</subject><subject>TOR protein</subject><issn>0028-646X</issn><issn>1469-8137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNp10c1u1DAUBWALgei0sOAFKkts6CKtncR_y2oEtFJFK1QkdpHHuZ6kSuzUdhhlxyPwjDwJplO6QKq98ObT0b0-CL2j5JTmc-am7pQqRvgLtKI1V4WklXiJVoSUsuA1_36ADmO8I4QoxsvX6KCSVFHBqxWa1kvypgt-BGzwAD9giFhbCybh1AG-vf6KJ526nV5w8jjAdh50ArwNfpc6rF2LR0h644c-jnh2LQQMDsJ2-f3zVwu2Nz24hI13bZ967-Ib9MrqIcLbx_cIffv08XZ9UVxdf75cn18VpqIVL0ytRQ01k62tdU15RYihdCNZK7hUIJgtNadMa21EWxKRVxOKKWas3VjN6-oIfdjnTsHfzxBTM_bRwDBoB36OTaloyfKVMtP3_9E7PweXp8uqrKikolRZneyVCT7GALaZQj_qsDSUNH9raHINzUMN2R4_Js6bEdon-e_fMzjbg10_wPJ8UvPl5mIf-QcCDpMC</recordid><startdate>202403</startdate><enddate>202403</enddate><creator>Canal, María Victoria</creator><creator>Mansilla, Natanael</creator><creator>Gras, Diana E.</creator><creator>Ibarra, Agustín</creator><creator>Figueroa, Carlos M.</creator><creator>Gonzalez, Daniel H.</creator><creator>Welchen, Elina</creator><general>Wiley Subscription Services, Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QO</scope><scope>7SN</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H95</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0009-0003-7726-395X</orcidid><orcidid>https://orcid.org/0000-0001-6052-3223</orcidid><orcidid>https://orcid.org/0000-0003-4025-573X</orcidid><orcidid>https://orcid.org/0000-0003-4047-0480</orcidid><orcidid>https://orcid.org/0000-0002-3137-8095</orcidid><orcidid>https://orcid.org/0009-0000-0874-1995</orcidid><orcidid>https://orcid.org/0009-0000-0690-6813</orcidid></search><sort><creationdate>202403</creationdate><title>Cytochrome c levels affect the TOR pathway to regulate growth and metabolism under energy‐deficient conditions</title><author>Canal, María Victoria ; 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Mitochondrial function is essential for plant growth, but the mechanisms involved in adjusting growth and metabolism to changes in mitochondrial energy production are not fully understood.
We studied plants with reduced expression of CYTC‐1, one of two genes encoding the respiratory chain component cytochrome c (CYTc) in Arabidopsis, to understand how mitochondria communicate their status to coordinate metabolism and growth.
Plants with CYTc deficiency show decreased mitochondrial membrane potential and lower ATP content, even when carbon sources are present. They also exhibit higher free amino acid content, induced autophagy, and increased resistance to nutritional stress caused by prolonged darkness, similar to plants with triggered starvation signals. CYTc deficiency affects target of rapamycin (TOR)‐pathway activation, reducing S6 kinase (S6K) and RPS6A phosphorylation, as well as total S6K protein levels due to increased protein degradation via proteasome and autophagy. TOR overexpression restores growth and other parameters affected in cytc‐1 mutants, even if mitochondrial membrane potential and ATP levels remain low.
We propose that CYTc‐deficient plants coordinate their metabolism and energy availability by reducing TOR‐pathway activation as a preventive signal to adjust growth in anticipation of energy exhaustion, thus providing a mechanism by which changes in mitochondrial activity are transduced to the rest of the cell.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>38191763</pmid><doi>10.1111/nph.19506</doi><tpages>2058</tpages><orcidid>https://orcid.org/0009-0003-7726-395X</orcidid><orcidid>https://orcid.org/0000-0001-6052-3223</orcidid><orcidid>https://orcid.org/0000-0003-4025-573X</orcidid><orcidid>https://orcid.org/0000-0003-4047-0480</orcidid><orcidid>https://orcid.org/0000-0002-3137-8095</orcidid><orcidid>https://orcid.org/0009-0000-0874-1995</orcidid><orcidid>https://orcid.org/0009-0000-0690-6813</orcidid></addata></record> |
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| ispartof | The New phytologist, 2024-03, Vol.241 (5), p.2039-2058 |
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| source | Wiley-Blackwell Journals |
| subjects | Adenosine Triphosphate - metabolism Amino acids Arabidopsis - metabolism Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Arabidopsis thaliana ATP Autophagy Biodegradation Carbon sources Cytochrome Cytochrome c Cytochromes Cytochromes c - genetics Cytochromes c - metabolism Darkness Electron transport Energy energy deficiency Energy metabolism Genes Kinases Membrane potential Membranes Metabolism Mitochondria Nutrient deficiency Phosphatidylinositol 3-Kinases - metabolism Phosphorylation Plant growth Plants Proteasomes Proteins Rapamycin Ribosomal Protein S6 Kinases - metabolism Sirolimus - pharmacology starvation target of rapamycin TOR protein |
| title | Cytochrome c levels affect the TOR pathway to regulate growth and metabolism under energy‐deficient conditions |
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