Exploring PIF4's contribution to early flowering in plants under daily variable temperature and its tissue‐specific flowering gene network

Abstract Molecular mechanisms of how constant temperatures affect flowering time have been largely characterized in the model plant Arabidopsis thaliana; however, the effect of natural daily variable temperature outside laboratories is only partly explored. Several flowering genes have been shown to...

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Main Authors: Jutapak Jenkitkonchai, Poppy Marriott, Weibing Yang, Napaporn Sriden, Jae‐Hoon Jung, Philip A. Wigge, Varodom Charoensawan
Format: Article
Language:English
Published: Wiley 2021-07-01
Series:Plant Direct
Subjects:
Online Access:https://doi.org/10.1002/pld3.339
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spelling doaj-e2c47e1f7d6e4675841304815ffc06d72021-10-06T14:05:26ZengWileyPlant Direct2475-44552021-07-0157n/an/a10.1002/pld3.339Exploring PIF4's contribution to early flowering in plants under daily variable temperature and its tissue‐specific flowering gene networkJutapak Jenkitkonchai0Poppy Marriott1Weibing Yang2Napaporn Sriden3Jae‐Hoon Jung4Philip A. Wigge5Varodom Charoensawan6Department of Biochemistry, Faculty of Science Mahidol University Bangkok ThailandThe Sainsbury Laboratory University of Cambridge Cambridge UKThe Sainsbury Laboratory University of Cambridge Cambridge UKDepartment of Biochemistry, Faculty of Science Mahidol University Bangkok ThailandThe Sainsbury Laboratory University of Cambridge Cambridge UKThe Sainsbury Laboratory University of Cambridge Cambridge UKDepartment of Biochemistry, Faculty of Science Mahidol University Bangkok ThailandAbstract Molecular mechanisms of how constant temperatures affect flowering time have been largely characterized in the model plant Arabidopsis thaliana; however, the effect of natural daily variable temperature outside laboratories is only partly explored. Several flowering genes have been shown to play important roles in temperature responses, including PHYTOCHROME‐INTERACTING FACTOR 4 (PIF4) and FLOWERING LOCUS C (FLC), the two genes encoding for the transcription factors (TFs) that act antagonistically to regulate flowering time by activating and repressing floral integrator FLOWERING LOCUS T (FT), respectively. In this study, we have taken a multidisciplinary approach to explore the contribution of PIF4 to the early flowering observed in the daily variable temperature (VAR) and to broaden its transcriptional network using publicly available transcriptomic data. We observed early flowering in the natural accessions Col‐0, C24 and their late flowering hybrid C24xCol grown under VAR, as compared with a constant temperature (CON). The loss‐of‐function mutation of PIF4 exhibits later flowering in VAR in both the Col‐0 parent and the C24xCol hybrid, suggesting that PIF4, at least in part, contributes to acceleration of flowering in the VAR condition. To investigate the interplay between PIF4 and its flowering regulator counterparts, FLC and FT, we performed transcriptional analyses and found that VAR increased PIF4 transcription at the end of the day when temperature peaked at 32°C, when FT transcription was also elevated. On the other hand, we observed a decrease in FLC transcription in the 4‐week‐old plants grown in VAR, as well as in the plants with PIF4 overexpression grown in CON. These results raise a possibility that PIF4 might also regulate FT indirectly through the repression of FLC, in addition to the well‐characterized direct control of PIF4 over FT. To further expand our view on the PIF4‐orientated flowering gene network in response to temperature changes, we have constructed a coexpression–transcriptional regulatory network by combining publicly available transcriptomic data and gene regulatory interactions of PIF4 and its closely related flowering genes, PIF5, FLC, and ELF3. The network model reveals conserved and tissue‐specific regulatory functions, which are useful for confirming as well as predicting the functions and regulatory interactions between these key flowering genes.https://doi.org/10.1002/pld3.339coexpression networkdaily temperature variationsFLOWERING LOCUS C (FLC)flowering timegene regulatory networkPHYTOCHROME‐INTERACTING FACTOR (PIF)
collection DOAJ
language English
format Article
sources DOAJ
author Jutapak Jenkitkonchai
Poppy Marriott
Weibing Yang
Napaporn Sriden
Jae‐Hoon Jung
Philip A. Wigge
Varodom Charoensawan
spellingShingle Jutapak Jenkitkonchai
Poppy Marriott
Weibing Yang
Napaporn Sriden
Jae‐Hoon Jung
Philip A. Wigge
Varodom Charoensawan
Exploring PIF4's contribution to early flowering in plants under daily variable temperature and its tissue‐specific flowering gene network
Plant Direct
coexpression network
daily temperature variations
FLOWERING LOCUS C (FLC)
flowering time
gene regulatory network
PHYTOCHROME‐INTERACTING FACTOR (PIF)
author_facet Jutapak Jenkitkonchai
Poppy Marriott
Weibing Yang
Napaporn Sriden
Jae‐Hoon Jung
Philip A. Wigge
Varodom Charoensawan
author_sort Jutapak Jenkitkonchai
title Exploring PIF4's contribution to early flowering in plants under daily variable temperature and its tissue‐specific flowering gene network
title_short Exploring PIF4's contribution to early flowering in plants under daily variable temperature and its tissue‐specific flowering gene network
title_full Exploring PIF4's contribution to early flowering in plants under daily variable temperature and its tissue‐specific flowering gene network
title_fullStr Exploring PIF4's contribution to early flowering in plants under daily variable temperature and its tissue‐specific flowering gene network
title_full_unstemmed Exploring PIF4's contribution to early flowering in plants under daily variable temperature and its tissue‐specific flowering gene network
title_sort exploring pif4's contribution to early flowering in plants under daily variable temperature and its tissue‐specific flowering gene network
publisher Wiley
series Plant Direct
issn 2475-4455
publishDate 2021-07-01
description Abstract Molecular mechanisms of how constant temperatures affect flowering time have been largely characterized in the model plant Arabidopsis thaliana; however, the effect of natural daily variable temperature outside laboratories is only partly explored. Several flowering genes have been shown to play important roles in temperature responses, including PHYTOCHROME‐INTERACTING FACTOR 4 (PIF4) and FLOWERING LOCUS C (FLC), the two genes encoding for the transcription factors (TFs) that act antagonistically to regulate flowering time by activating and repressing floral integrator FLOWERING LOCUS T (FT), respectively. In this study, we have taken a multidisciplinary approach to explore the contribution of PIF4 to the early flowering observed in the daily variable temperature (VAR) and to broaden its transcriptional network using publicly available transcriptomic data. We observed early flowering in the natural accessions Col‐0, C24 and their late flowering hybrid C24xCol grown under VAR, as compared with a constant temperature (CON). The loss‐of‐function mutation of PIF4 exhibits later flowering in VAR in both the Col‐0 parent and the C24xCol hybrid, suggesting that PIF4, at least in part, contributes to acceleration of flowering in the VAR condition. To investigate the interplay between PIF4 and its flowering regulator counterparts, FLC and FT, we performed transcriptional analyses and found that VAR increased PIF4 transcription at the end of the day when temperature peaked at 32°C, when FT transcription was also elevated. On the other hand, we observed a decrease in FLC transcription in the 4‐week‐old plants grown in VAR, as well as in the plants with PIF4 overexpression grown in CON. These results raise a possibility that PIF4 might also regulate FT indirectly through the repression of FLC, in addition to the well‐characterized direct control of PIF4 over FT. To further expand our view on the PIF4‐orientated flowering gene network in response to temperature changes, we have constructed a coexpression–transcriptional regulatory network by combining publicly available transcriptomic data and gene regulatory interactions of PIF4 and its closely related flowering genes, PIF5, FLC, and ELF3. The network model reveals conserved and tissue‐specific regulatory functions, which are useful for confirming as well as predicting the functions and regulatory interactions between these key flowering genes.
topic coexpression network
daily temperature variations
FLOWERING LOCUS C (FLC)
flowering time
gene regulatory network
PHYTOCHROME‐INTERACTING FACTOR (PIF)
url https://doi.org/10.1002/pld3.339
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