Arabidopsis TCP4 Transcription Factor Inhibits High Temperature-induced Homeotic Conversion of Ovules

Overview

Journal Nat Commun

Specialty Biology

Date 2023 Sep 13

PMID 37704599

Authors

Jingqiu Lan

Ning Wang

Yutao Wang

Yidan Jiang

Hao Yu

Xiaofeng Cao

Genji Qin

Affiliations

Soon will be listed here.

Abstract

Abnormal high temperature (HT) caused by global warming threatens plant survival and food security, but the effects of HT on plant organ identity are elusive. Here, we show that Class II TEOSINTE BRANCHED 1/CYCLOIDEA/ PCF (TCP) transcription factors redundantly protect ovule identity under HT. The duodecuple tcp2/3/4/5/10/13/17/24/1/12/18/16 (tcpDUO) mutant displays HT-induced ovule conversion into carpelloid structures. Expression of TCP4 in tcpDUO complements the ovule identity conversion. TCP4 interacts with AGAMOUS (AG), SEPALLATA3 (SEP3), and the homeodomain transcription factor BELL1 (BEL1) to strengthen the association of BEL1 with AG-SEP3. The tcpDUO mutant synergistically interacts with bel1 and the ovule identity gene seedstick (STK) mutant stk in tcpDUO bel1 and tcpDUO stk. Our findings reveal the critical roles of Class II TCPs in maintaining ovule identity under HT and shed light on the molecular mechanisms by which ovule identity is determined by the integration of internal factors and environmental temperature.

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References

Ge C, Ye J, Weber C, Sun W, Zhang H, Zhou Y . The histone demethylase KDM6B regulates temperature-dependent sex determination in a turtle species. Science. 2018; 360(6389):645-648. DOI: 10.1126/science.aap8328. View

Ray A, Robinson-Beers K, Ray S, Baker S, Lang J, Preuss D . Arabidopsis floral homeotic gene BELL (BEL1) controls ovule development through negative regulation of AGAMOUS gene (AG). Proc Natl Acad Sci U S A. 1994; 91(13):5761-5. PMC: 44076. DOI: 10.1073/pnas.91.13.5761. View

Rodriguez-Cazorla E, Ripoll J, Ortuno-Miquel S, Martinez-Laborda A, Vera A . Dissection of the Arabidopsis HUA-PEP gene activity reveals that ovule fate specification requires restriction of the floral A-function. New Phytol. 2020; 227(4):1222-1234. DOI: 10.1111/nph.16589. View

Lan J, Zhang J, Yuan R, Yu H, An F, Sun L . TCP transcription factors suppress cotyledon trichomes by impeding a cell differentiation-regulating complex. Plant Physiol. 2021; 186(1):434-451. PMC: 8154074. DOI: 10.1093/plphys/kiab053. View

Huang T, Irish V . Temporal Control of Plant Organ Growth by TCP Transcription Factors. Curr Biol. 2015; 25(13):1765-70. DOI: 10.1016/j.cub.2015.05.024. View

Alvarez J, Smyth D . CRABS CLAW and SPATULA, two Arabidopsis genes that control carpel development in parallel with AGAMOUS. Development. 1999; 126(11):2377-86. DOI: 10.1242/dev.126.11.2377. View

Lee S, Wang W, Huq E . Spatial regulation of thermomorphogenesis by HY5 and PIF4 in Arabidopsis. Nat Commun. 2021; 12(1):3656. PMC: 8209091. DOI: 10.1038/s41467-021-24018-7. View

Doebley J, Stec A, Gustus C . teosinte branched1 and the origin of maize: evidence for epistasis and the evolution of dominance. Genetics. 1995; 141(1):333-46. PMC: 1206731. DOI: 10.1093/genetics/141.1.333. View

Tao Q, Guo D, Wei B, Zhang F, Pang C, Jiang H . The TIE1 transcriptional repressor links TCP transcription factors with TOPLESS/TOPLESS-RELATED corepressors and modulates leaf development in Arabidopsis. Plant Cell. 2013; 25(2):421-37. PMC: 3608769. DOI: 10.1105/tpc.113.109223. View

10.

Yamada T, Sasaki Y, Hashimoto K, Nakajima K, Gasser C . CORONA, PHABULOSA and PHAVOLUTA collaborate with BELL1 to confine WUSCHEL expression to the nucellus in Arabidopsis ovules. Development. 2015; 143(3):422-6. DOI: 10.1242/dev.129833. View

11.

Schneitz K, Hulskamp M, Kopczak S, Pruitt R . Dissection of sexual organ ontogenesis: a genetic analysis of ovule development in Arabidopsis thaliana. Development. 1997; 124(7):1367-76. DOI: 10.1242/dev.124.7.1367. View

12.

Brambilla V, Kater M, Colombo L . Ovule integument identity determination in Arabidopsis. Plant Signal Behav. 2009; 3(4):246-7. PMC: 2634191. DOI: 10.4161/psb.3.4.5175. View

13.

Wang J, Chen H . A novel CRISPR/Cas9 system for efficiently generating Cas9-free multiplex mutants in . aBIOTECH. 2022; 1(1):6-14. PMC: 9584096. DOI: 10.1007/s42994-019-00011-z. View

14.

Nath U, Crawford B, Carpenter R, Coen E . Genetic control of surface curvature. Science. 2003; 299(5611):1404-7. DOI: 10.1126/science.1079354. View

15.

Efroni I, Blum E, Goldshmidt A, Eshed Y . A protracted and dynamic maturation schedule underlies Arabidopsis leaf development. Plant Cell. 2008; 20(9):2293-306. PMC: 2570723. DOI: 10.1105/tpc.107.057521. View

16.

Modrusan Z, Reiser L, Feldmann K, Fischer R, Haughn G . Homeotic Transformation of Ovules into Carpel-like Structures in Arabidopsis. Plant Cell. 1994; 6(3):333-349. PMC: 160437. DOI: 10.1105/tpc.6.3.333. View

17.

Crawford B, Nath U, Carpenter R, Coen E . CINCINNATA controls both cell differentiation and growth in petal lobes and leaves of Antirrhinum. Plant Physiol. 2004; 135(1):244-53. PMC: 429364. DOI: 10.1104/pp.103.036368. View

18.

Viola I, Reinheimer R, Ripoll R, Uberti Manassero N, Gonzalez D . Determinants of the DNA binding specificity of class I and class II TCP transcription factors. J Biol Chem. 2011; 287(1):347-356. PMC: 3249086. DOI: 10.1074/jbc.M111.256271. View

19.

Ibanez C, Delker C, Martinez C, Burstenbinder K, Janitza P, Lippmann R . Brassinosteroids Dominate Hormonal Regulation of Plant Thermomorphogenesis via BZR1. Curr Biol. 2018; 28(2):303-310.e3. DOI: 10.1016/j.cub.2017.11.077. View

20.

Bowman J, Drews G, Meyerowitz E . Expression of the Arabidopsis floral homeotic gene AGAMOUS is restricted to specific cell types late in flower development. Plant Cell. 1991; 3(8):749-58. PMC: 160042. DOI: 10.1105/tpc.3.8.749. View