Stoma-to-stomach evolution: the hidden link between stomatal physiology and plant carnivory
Final Report Abstract
Carnivorous pitcher plants secrete acidic digestive fluids akin to animal gastric juices. However, the evolutionary origins of their ability for acid secretion, despite originally lacking stomach-like organs, has been unclear. Here, we show that the digestive glands of the Australian pitcher plant Cephalotus follicularis have adapted stomatal ion transport mechanisms used originally for osmolality regulation allowing stomatal movement, to acidify digestive fluid. Our findings indicate that the production of digestive fluid in pitcher plants is a two-step process; Large multicellular glands first secrete a pH-neutral fluid into the pitcher lumen, which is subsequently acidified by small bicellular glands resembling stomatal guard cells. Our transcriptome analysis of enriched small gland cells showed high transcript abundance of the proton-pump H+-ATPase 1 (HA1), the chloride/nitrate channel SLAC1 HOLOLOGUE 3 (SLAH3), and the nitrate-preferential transporter NRT1/PTR FAMILY 6.3 (NPF6.3), alongside low expression of other well-known ion transport proteins common in guard cell plasma membranes. Electrophysiological measurements on Xenopus oocytes validated the proton export activity of CfHA1, and its inhibitor attenuated fluid acidification in Cephalotus pitchers. CfSLAH3 transports both chloride and nitrate, suggesting that CfNPF6.3 may reabsorb nitrate and thereby establish chloride as the primary counter-ion. These findings illustrate how an ancient molecular mechanism is adapted for a distinctly novel cellular function.
Publications
-
The digestive systems of carnivorous plants. Plant Physiology, 190(1), 44-59.
Freund, Matthias; Graus, Dorothea; Fleischmann, Andreas; Gilbert, Kadeem J.; Lin, Qianshi; Renner, Tanya; Stigloher, Christian; Albert, Victor A.; Hedrich, Rainer & Fukushima, Kenji
-
Subgenome dominance shapes novel gene evolution in the decaploid pitcher plant Nepenthes gracilis. Nature Plants, 9(12), 2000-2015.
Saul, Franziska; Scharmann, Mathias; Wakatake, Takanori; Rajaraman, Sitaram; Marques, André; Freund, Matthias; Bringmann, Gerhard; Channon, Louisa; Becker, Dirk; Carroll, Emily; Low, Yee Wen; Lindqvist, Charlotte; Gilbert, Kadeem J.; Renner, Tanya; Masuda, Sachiko; Richter, Michaela; Vogg, Gerd; Shirasu, Ken; Michael, Todd P. ... & Fukushima, Kenji
