Modulation of warm temperature-sensitive growth using a phytochrome B dark reversion variant, phyB[G515E], in Arabidopsis and rice

• Published in: Journal of advanced research 2024-09, Vol.63, p.57-72
• Main Authors: Jeon, Jin, Rahman, Md Mizanor, Yang, Hee Wook, Kim, Jaewook, Gam, Ho-Jun, Song, Ji Young, Jeong, Seok Won, Kim, Jeong-Il, Choi, Myoung-Goo, Shin, Dong-Ho, Choi, Giltsu, Shim, Donghwan, Jung, Jae-Hoon, Lee, In-Jung, Jeon, Jong-Seong, Park, Youn-Il
• Format: Article
• Language: English
• Subjects: Arabidopsis; Arabidopsis - genetics; Arabidopsis - growth & development; Arabidopsis - metabolism; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Basic and Biological Science; Basic Helix-Loop-Helix Transcription Factors - genetics; Basic Helix-Loop-Helix Transcription Factors - metabolism; Gene Expression Regulation, Plant; Heat shock-inducible promoters; Hot Temperature; Hypocotyl - genetics; Hypocotyl - growth & development; Hypocotyl - metabolism; Indoleacetic Acids - metabolism; Oryza - genetics; Oryza - growth & development; Oryza - metabolism; Phytochrome B - genetics; Phytochrome B - metabolism; Phytochrome B dark reversion variants; PIF4; Plants, Genetically Modified - genetics; Plants, Genetically Modified - growth & development; Plants, Genetically Modified - metabolism; Rice; Seedlings - genetics; Seedlings - growth & development; Seedlings - metabolism; Signal Transduction; Temperature; Thermomorphogenic response
• ISSN: 2090-1232; 2090-1224
• DOI: 10.1016/j.jare.2023.11.001

[Display omitted] •Phytochrome B variant phyB[G515E] with a slow dark reversion was generated.•phyB[G515E] forms warm temperature-insensitive nuclear photobodies.•PHYB[G515E] expression inhibited the phytochrome interacting factor4-auxin pathway.•PHYB[G515E] transgenic Arabidopsis and rice showed warming-insensitive growth.•phyB[G515E] is a powerful tool for engineering warm temperature-insensitive crops. Ambient temperature-induced hypocotyl elongation in Arabidopsis seedlings is sensed by the epidermis-localized phytochrome B (phyB) and transduced into auxin biosynthesis via a basic helix-loop-helix transcription factor, phytochrome-interacting factor 4 (PIF4). Once synthesized, auxin travels down from the cotyledons to the hypocotyl, triggering hypocotyl cell elongation. Thus, the phyB–PIF4 module involved in thermosensing and signal transduction is a potential genetic target for engineering warm temperature-insensitive plants. This study aims to manipulate warm temperature-induced elongation of plants at the post-translational level using phyB variants with dark reversion, the expression of which is subjected to heat stress. The thermosensitive growth response of Arabidopsis was manipulated by expressing the single amino acid substitution variant of phyB (phyB[G515E]), which exhibited a lower dark reversion rate than wild-type phyB. Other variants with slow (phyB[G564E]) or rapid (phyB[S584F]) dark reversion or light insensitivity (phyB[G767R]) were also included in this study for comparison. Warming-induced transient expression of phyB variants was achieved using heat shock-inducible promoters. Arabidopsis PHYB[G515E] and PHYB[G564E] were also constitutively expressed in rice in an attempt to manipulate the heat sensitivity of a monocotyledonous plant species. At an elevated temperature, Arabidopsis seedlings transiently expressing PHYB[G515E] under the control of a heat shock-inducible promoter exhibited shorter hypocotyls than those expressing PHYB and other PHYB variant genes. This warm temperature-insensitive growth was related to the lowered PIF4 and auxin responses. In addition, transgenic rice seedlings expressing Arabidopsis PHYB[G515E] and PHYB[G564E] showed warm temperature-insensitive shoot growth. Transient expression of phyB variants with altered dark reversion rates could serve as an effective optogenetic technique for manipulating PIF4–auxin-mediated thermomorphogenic responses in plants.