Evolution of Sexual Reproduction in Plants
Final Report Abstract
Modern life depends on flowering plants for food, fuel, textiles, and building materials. However, our capacity to generate sufficient food, animal feed and energy is increasingly compromised by human population expansion, competition for land use, rapid biodiversity loss and predicted global climate change. It is therefore crucial to study the process of sexual reproduction in higher plants to overcome fertilization barriers and to enhance crop productivity. The EVOREPRO project delivers the first comprehensive view of the molecular evolution of plant sexual reproduction and provides insights into the origins of double fertilization in flowering plants. To this end the eight partner laboratories from Europe and the US have taken a comparative gene expression-based approach to investigate regulatory networks underlying sexual reproduction across Marchantia, Physcomitrella, Amborella, Arabidopsis and a range of crop species. The aim was to identify novel and missing key components involved in gamete development and fertilization processes such as germ cell division and specification, gamete interaction and activation, as well as chromatin re-programming and epigenetic inheritance in these cells. The consortium partners have produced novel RNAseq data sets covering gametogenesis, not only for the angiosperm Arabidopsis and the bryophyte Physcomitrella, but also for the first time for the basal angiosperm Amborella. These data sets together with additional ones for the project’s target species comprise the backbone of the EVOREPRO database which was developed to study evolutionary changes in co-expression networks. Analysis of the Amborella egg apparatus transcriptome has already provided unprecedented insights into conserved molecular mechanisms and the evolution of fertilization-related genes. In addition, we have reported functional conservation of the transcription factor DUO1, which is essential for male gametogenesis in bryophytes and angiosperms. Furthermore, the evolution of the membrane insertion motifs of HAP2, a eukaryotic gamete fusogen, was elucidated. In Arabidopsis, a complex mechanism that selectively reprograms H3K27me3 in sperm chromatin has been discovered. This mechanism not only enables expression of the gene network responsible for sperm differentiation, but also primes expression of key genes for several developmental transitions in the next generation. The EVOREPRO database and novel molecular tool sets, including cell-type specific marker lines and methods to study the changes of chromatin states and gene expression levels taking place during gametogenesis, are instrumental in taking research on plant sexual reproduction to the next level. The most recent updates can be found on the project’s webpage: www.evorepro.org
Publications
- (2018) Evolutionary diversification of the HAP2 membrane insertion motifs to drive gamete fusion across eukaryotes. PLoS Biol. 16: e2006357
Fedry J, Forcina J, Legrand P, Péhau-Arnaudet G, Haouz A, Johnson MA, Rey FA, Krey T
(See online at https://doi.org/10.1371/journal.pbio.2006357) - (2018) Highly efficient heritable targeted deletions of gene clusters and non-coding regulatory regions in Arabidopsis using CRISPR/Cas9. Sci. Rep 8: 4443-4454
Durr J, Papareddy R, Nakajima K, Gutierrez-Marcos JF
(See online at https://doi.org/10.1038/s41598-018-22667-1) - (2018) New cues for body axis formation in plant embryos. Curr Opin Plant Biol 47: 16-21
Ueda M, Berger F
(See online at https://doi.org/10.1016/j.pbi.2018.08.005) - (2018) Partial maintenance of organ-specific epigenetic marks during plant asexual reproduction leads to heritable phenotypic variation. PNAS 115: E9145– E9152
Wibowo A, Becker C, Durr J, Price J, Spaepen S, Hilton S, Putra H, Papareddy R, Saintain Q, Harvey S, Bending GD, Schulze-Lefert P, Weigel D, Gutierrez-Marcos J
(See online at https://doi.org/10.1073/pnas.1805371115) - (2019) A Fruitful Journey: Pollen Tube Navigation from Germination to Fertilization. Annu. Rev. Plant Biol.
Johnson MA, Harper JF, Palanivelu, R
(See online at https://doi.org/10.1146/annurev-arplant-050718-100133) - (2019) A simple and robust protocol for immunostaining Arabidopsis pollen nuclei. Plant Reprod. 32: 39–43
Borg M, Buendia D, Berger F
(See online at https://doi.org/10.1007/s00497-018-00360-7) - (2019) Iterative subtraction facilitates automated, quantitative analysis of multiple pollen tube growth features. Plant Reprod. 32: 45–54
Ponvert N, Goldberg J, Leydon A, Johnson MA
(See online at https://doi.org/10.1007/s00497-018-00351-8) - (2019) Kingdom-wide comparison reveals the evolution of diurnal gene expression in Archaeplastida. Nat. Commun. 10: 737
Ferrari C, Proost S, Janowski M, Becker J, Nikoloski Z, Bhattacharya D, Price D, Tohge T, Bar-Even A, Fernie A, Stitt M, Mutwil M
(See online at https://doi.org/10.1038/s41467-019-08703-2) - (2019) Specific chromatin changes mark lateral organ founder cells in the Arabidopsis thaliana inflorescence meristem. J. Exp. Bot.
Frerichs A, Engelhorn J, Altmüller J, Gutierrez-Marcos JF, Werr W
(See online at https://doi.org/10.1093/jxb/erz181) - (2019) The evolution and patterning of male gametophyte development. Curr. Top. Dev. Biol. 131: 257-298
Hackenberg D, Twell D
(See online at https://doi.org/10.1016/bs.ctdb.2018.10.008) - (2019) Transcriptomics of Arabidopsis sperm cells at single-cell resolution. Plant Reprod. 32: 29–38
Misra CS, Santos MR, Rafael-Fernandes M, Martins NP, Monteiro M, Becker JD
(See online at https://doi.org/10.1007/s00497-018-00355-4) - (2019) Transcriptomics of manually isolated Amborella trichopoda egg apparatus cells. Plant Reprod. 32: 15–27
Flores-Tornero M, Proost S, Mutwil M, Scutt CP, Dresselhaus T, Sprunck S
(See online at https://doi.org/10.1007/s00497-019-00361-0)
