Abscisic acid controlled sex before transpiration in vascular plants
Monday, 2016/11/14 | 07:54:22
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Scott A. M. McAdam, Timothy J. Brodribb, Jo Ann Banks, Rainer Hedrich, Nadia M. Atallah, Chao Cai, Michael A. Geringer, Christof Lind, David S. Nichols, Kye Stachowski, Dietmar Geiger, and Frances C. Sussmilch SignificanceSince the dawn of land plants, the phytohormone abscisic acid (ABA) has played a critical role in regulating plant responses to water availability. Here we seek to explain the origins of the core ABA signaling pathway found in modern seed plants. Using the characterization of mutants and gene silencing in a fern species, we find that the same hormone signaling components are used in sex determination of ferns as are used for the control of seed dormancy and transpiration in seed plants. Ferns are shown to lack downstream functionality of stomatal components, suggesting that the origins of the core ABA signaling pathway in seed plants may lie in the sexual differentiation of ferns. AbstractSexual reproduction in animals and plants shares common elements, including sperm and egg production, but unlike animals, little is known about the regulatory pathways that determine the sex of plants. Here we use mutants and gene silencing in a fern species to identify a core regulatory mechanism in plant sexual differentiation. A key player in fern sex differentiation is the phytohormone abscisic acid (ABA), which regulates the sex ratio of male to hermaphrodite tissues during the reproductive cycle. Our analysis shows that in the fern Ceratopteris richardii, a gene homologous to core ABA transduction genes in flowering plants [SNF1-related kinase2s (SnRK2s)] is primarily responsible for the hormonal control of sex determination. Furthermore, we provide evidence that this ABA–SnRK2 signaling pathway has transitioned from determining the sex of ferns to controlling seed dormancy in the earliest seed plants before being co-opted to control transpiration and CO2 exchange in derived seed plants. By tracing the evolutionary history of this ABA signaling pathway from plant reproduction through to its role in the global regulation of plant–atmosphere gas exchange during the last 450 million years, we highlight the extraordinary effect of the ABA–SnRK2 signaling pathway in plant evolution and vegetation function.
See: http://www.pnas.org/content/113/45/12862.full PNAS November 8 2016; vol.113; no.45: 12862–12867
Fig. 1. GAIA1, a C. richardii homolog of OST1, regulates ABA signaling for gametophyte sex determination. (A) C. richardii sporophyte. (B) Gametophyte phenotype for wild-type (Hn-n) and gaia1 mutant alleles grown on media containing ACE and 10 µM ABA, with diagrams showing GAIA1 gene and predicted protein structure for each allele, indicating the nature of mutations. No portion of GAIA1 could be isolated from gaia1-3 (SI Appendix, Fig. S3). (Scale bars, 200 µm, 100 bp, or 10 aa; gene/protein diagrams share the same scale.) (C) Phenotypes of three representative gametophytes bombarded with only 35S::DsRed2 acting as controls and three GAIA1 RNAi gametophytes cobombarded with both 35S::DsRed2 and 35S::hpGAIA1. Knocking down the expression of GAIA1 prevents the development of a new hermaphroditic prothallus (indicated by arrows in the controls) when plants are transferred from media containing only ACE to media containing both ACE and 5 µM ABA. (Scale bars, 200 µm.) (D) Phylogram of C. richardii (Cr), Oryza sativa (Os), and A. thaliana (At) SnRK2-type protein kinases, with Vicia faba (Vf) AAPK also included. The OST1-type subgroup is shaded in blue with the names of ABA-signaling proteins associated with stomatal control in blue text, proteins acting in seed dormancy in green, and proteins linked to both processes in blue and underlined in green. CrGAIA1 is shown in red. Branches with bootstrap values <50% obtained from 1,000 trees have been collapsed. Representative Arabidopsis SnRK1 and SnRK3 proteins are included as outgroups. Phylogenetic analysis is based on the sequence alignment in SI Appendix, Dataset. For sequence details, see SI Appendix, Dataset. (E) Alignments showing residues in the αC-helix of the kinase domain and ABA box conserved among OST1 homologs and between SnRK2 proteins. Shading indicates degree of conservation (black = 60%, dark gray = 50%, and light gray = 40%, yellow = residues affected in gaia1 mutants). Protein names are colored as in D.
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