A cis-carotene derived apocarotenoid regulates etioplast and chloroplast development
Carotenoids are a core plastid component and yet their regulatory function during plastid biogenesis remains enigmatic. A unique carotenoid biosynthesis mutant, carotenoid chloroplast regulation 2 (ccr2), that has no prolamellar body (PLB) and normal PROTOCHLOROPHYLLIDE OXIDOREDUCTASE (POR) levels,...
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2020-01-01
|
| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/45310 |
| _version_ | 1818026806403399680 |
|---|---|
| author | Christopher I Cazzonelli Xin Hou Yagiz Alagoz John Rivers Namraj Dhami Jiwon Lee Shashikanth Marri Barry J Pogson |
| author_facet | Christopher I Cazzonelli Xin Hou Yagiz Alagoz John Rivers Namraj Dhami Jiwon Lee Shashikanth Marri Barry J Pogson |
| author_sort | Christopher I Cazzonelli |
| collection | DOAJ |
| description | Carotenoids are a core plastid component and yet their regulatory function during plastid biogenesis remains enigmatic. A unique carotenoid biosynthesis mutant, carotenoid chloroplast regulation 2 (ccr2), that has no prolamellar body (PLB) and normal PROTOCHLOROPHYLLIDE OXIDOREDUCTASE (POR) levels, was used to demonstrate a regulatory function for carotenoids and their derivatives under varied dark-light regimes. A forward genetics approach revealed how an epistatic interaction between a ζ-carotene isomerase mutant (ziso-155) and ccr2 blocked the biosynthesis of specific cis-carotenes and restored PLB formation in etioplasts. We attributed this to a novel apocarotenoid retrograde signal, as chemical inhibition of carotenoid cleavage dioxygenase activity restored PLB formation in ccr2 etioplasts during skotomorphogenesis. The apocarotenoid acted in parallel to the repressor of photomorphogenesis, DEETIOLATED1 (DET1), to transcriptionally regulate PROTOCHLOROPHYLLIDE OXIDOREDUCTASE (POR), PHYTOCHROME INTERACTING FACTOR3 (PIF3) and ELONGATED HYPOCOTYL5 (HY5). The unknown apocarotenoid signal restored POR protein levels and PLB formation in det1, thereby controlling plastid development. |
| first_indexed | 2024-12-10T04:37:51Z |
| format | Article |
| id | doaj.art-c975e25aca6145efa5ee2340fefdc005 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-12-10T04:37:51Z |
| publishDate | 2020-01-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-c975e25aca6145efa5ee2340fefdc0052022-12-22T02:01:57ZengeLife Sciences Publications LtdeLife2050-084X2020-01-01910.7554/eLife.45310A cis-carotene derived apocarotenoid regulates etioplast and chloroplast developmentChristopher I Cazzonelli0https://orcid.org/0000-0003-3096-3193Xin Hou1https://orcid.org/0000-0003-4625-1692Yagiz Alagoz2https://orcid.org/0000-0001-5081-6874John Rivers3https://orcid.org/0000-0002-7500-5637Namraj Dhami4https://orcid.org/0000-0002-6014-3500Jiwon Lee5Shashikanth Marri6Barry J Pogson7https://orcid.org/0000-0003-1869-2423Hawkesbury Institute for the Environment, Western Sydney University, Penrith, AustraliaResearch School of Biology, The Australian National University, Canberra, AustraliaHawkesbury Institute for the Environment, Western Sydney University, Penrith, AustraliaResearch School of Biology, The Australian National University, Canberra, AustraliaHawkesbury Institute for the Environment, Western Sydney University, Penrith, AustraliaCentre for Advanced Microscopy, The Australian National University, Canberra, AustraliaResearch School of Biology, The Australian National University, Canberra, AustraliaResearch School of Biology, The Australian National University, Canberra, AustraliaCarotenoids are a core plastid component and yet their regulatory function during plastid biogenesis remains enigmatic. A unique carotenoid biosynthesis mutant, carotenoid chloroplast regulation 2 (ccr2), that has no prolamellar body (PLB) and normal PROTOCHLOROPHYLLIDE OXIDOREDUCTASE (POR) levels, was used to demonstrate a regulatory function for carotenoids and their derivatives under varied dark-light regimes. A forward genetics approach revealed how an epistatic interaction between a ζ-carotene isomerase mutant (ziso-155) and ccr2 blocked the biosynthesis of specific cis-carotenes and restored PLB formation in etioplasts. We attributed this to a novel apocarotenoid retrograde signal, as chemical inhibition of carotenoid cleavage dioxygenase activity restored PLB formation in ccr2 etioplasts during skotomorphogenesis. The apocarotenoid acted in parallel to the repressor of photomorphogenesis, DEETIOLATED1 (DET1), to transcriptionally regulate PROTOCHLOROPHYLLIDE OXIDOREDUCTASE (POR), PHYTOCHROME INTERACTING FACTOR3 (PIF3) and ELONGATED HYPOCOTYL5 (HY5). The unknown apocarotenoid signal restored POR protein levels and PLB formation in det1, thereby controlling plastid development.https://elifesciences.org/articles/45310carotenoidtranscriptional regulationapocarotenoid signalprolamellar bodyetioplastretrograde signal |
| spellingShingle | Christopher I Cazzonelli Xin Hou Yagiz Alagoz John Rivers Namraj Dhami Jiwon Lee Shashikanth Marri Barry J Pogson A cis-carotene derived apocarotenoid regulates etioplast and chloroplast development eLife carotenoid transcriptional regulation apocarotenoid signal prolamellar body etioplast retrograde signal |
| title | A cis-carotene derived apocarotenoid regulates etioplast and chloroplast development |
| title_full | A cis-carotene derived apocarotenoid regulates etioplast and chloroplast development |
| title_fullStr | A cis-carotene derived apocarotenoid regulates etioplast and chloroplast development |
| title_full_unstemmed | A cis-carotene derived apocarotenoid regulates etioplast and chloroplast development |
| title_short | A cis-carotene derived apocarotenoid regulates etioplast and chloroplast development |
| title_sort | cis carotene derived apocarotenoid regulates etioplast and chloroplast development |
| topic | carotenoid transcriptional regulation apocarotenoid signal prolamellar body etioplast retrograde signal |
| url | https://elifesciences.org/articles/45310 |
| work_keys_str_mv | AT christophericazzonelli aciscarotenederivedapocarotenoidregulatesetioplastandchloroplastdevelopment AT xinhou aciscarotenederivedapocarotenoidregulatesetioplastandchloroplastdevelopment AT yagizalagoz aciscarotenederivedapocarotenoidregulatesetioplastandchloroplastdevelopment AT johnrivers aciscarotenederivedapocarotenoidregulatesetioplastandchloroplastdevelopment AT namrajdhami aciscarotenederivedapocarotenoidregulatesetioplastandchloroplastdevelopment AT jiwonlee aciscarotenederivedapocarotenoidregulatesetioplastandchloroplastdevelopment AT shashikanthmarri aciscarotenederivedapocarotenoidregulatesetioplastandchloroplastdevelopment AT barryjpogson aciscarotenederivedapocarotenoidregulatesetioplastandchloroplastdevelopment AT christophericazzonelli ciscarotenederivedapocarotenoidregulatesetioplastandchloroplastdevelopment AT xinhou ciscarotenederivedapocarotenoidregulatesetioplastandchloroplastdevelopment AT yagizalagoz ciscarotenederivedapocarotenoidregulatesetioplastandchloroplastdevelopment AT johnrivers ciscarotenederivedapocarotenoidregulatesetioplastandchloroplastdevelopment AT namrajdhami ciscarotenederivedapocarotenoidregulatesetioplastandchloroplastdevelopment AT jiwonlee ciscarotenederivedapocarotenoidregulatesetioplastandchloroplastdevelopment AT shashikanthmarri ciscarotenederivedapocarotenoidregulatesetioplastandchloroplastdevelopment AT barryjpogson ciscarotenederivedapocarotenoidregulatesetioplastandchloroplastdevelopment |