June 30, 2017
Purdue research reveals plant volatiles released more deliberately than once thought
WEST LAFAYETTE, Ind. — A Purdue University team of scientists upended a long-held assumption about how plant volatile compounds, the chemicals that are responsible for scent, move to the outside of the cells to attract pollinators, defend the plant and perform other key functions.
Natalia Dudareva, distinguished professor of biochemistry and the project’s principal investigator, said volatile compounds are actively trafficked out of cells through the use of an ATP-binding cassette transporter (ABC transporter), which moves substances across cell membranes. She worked with John Morgan, professor of chemical engineering, and Joshua Widhalm, a Purdue assistant professor of horticulture, and Funmilayo Adebesin, a doctoral student in Purdue’s Department of Biochemistry, as well as collaborators at the Université Catholique de Louvain and the University of Amsterdam.
“People assumed emission of volatile compounds from plant tissues was simple diffusion. Nobody considered it could be active transport,” said Dudareva, whose findings were published in the journal Science.
If diffused, volatile compounds would simply move in an unregulated manner from areas of high concentration inside the cells to low concentration outside the cells. But since the process requires an ABC transporter, that means the buildup and release of these compounds could be modified to help plants overcome effects of climate change on volatile emission, for example.
“If we want to increase pollination or improve plant defense, we need to know what we need to manipulate,” Dudareva said. “Volatiles also protect plants against abiotic stresses — light, temperature and oxidative stresses — and volatiles play a significant role in the atmosphere.”
Morgan said to uncover the method for volatile transport, the researchers reasoned that in a diffusion-based model the compounds should reside in a hydrophobic environment such as a cell membrane. But he knew that there would be far too many accumulating in membranes, causing damage, if they were exclusively diffusing.
That led the team to consider whether a transporter was involved. Widhalm said he looked at petunia gene expression observed at the bud stage, when hardly any volatiles are released, and at the second day of flowering, when volatile release is at its height. They observed a significant difference in the expression of the gene that controls the ABC transporter.
Adebesin then suppressed the transporter gene and observed a significant decrease in the amount of volatiles emitted. With reduced active transport, the volatile compounds accumulated inside of the cells and were found to destroy cell membranes, as the team had hypothesized.
The finding is one significant factor in the processes controlling creation and emission of volatile compounds.
“This is one step of many barriers with which volatiles have to pass through,” Morgan said. “To mathematically model the transport, we do need to uncover the other factors. There are several barriers that horses have to jump over gates to get out of the pen — and this is one of those gates.”
Next, the researchers plan to go one step back in the process to determine how volatile compounds make their way to cell membranes. The National Science Foundation, the Belgian National Fund for Scientific Research and the Interuniversity Poles of Attraction Program funded the research.
Writer: Brian Wallheimer, 765-532-0233, brian.wallheimer@gmail.com
Contact: Shari Finnell, sfinnell@purdue.edu
Source: Natalia Dudareva, 765-494-1325, dudareva@purdue.edu
John Morgan, 765-494-4088, jamorgan@purdue.edu
Josh Widhalm, 765-496-3891, jwidhalm@purdue.edu
Funmilayo Adebesin, fadebesi@purdue.edu
ABSTRACT
Emission of volatile organic compounds from petunia is facilitated by an ABC transporter
Funmilayo Adebesin1, Joshua R. Widhalm1,2,†, Benoît Boachon1, François Lefèvre3, Baptiste Pierman3, Joseph H. Lynch1, Iftekhar Alam3,§, Bruna Junqueira3, Ryan Benke1, Shaunak Ray4, Justin A. Porter5, Makoto Yanagisawa6, Hazel Y. Wetzstein5, John A. Morgan1,4, Marc Boutry3, Robert C. Schuurink7 & Natalia Dudareva1,2,5,*
1 Department of Biochemistry, Purdue University, West Lafayette, IN
2 Purdue Center for Plant Biology, Purdue University, West Lafayette, IN
3 Institut des Sciences de la Vie, Université catholique de Louvain, Croix du Sud, 4-5, Box L7-04-14, 1348 Louvain-la-Neuve, Belgium
4 School of Chemical Engineering, Purdue University, 480 Stadium Mall Dr., West Lafayette, IN
5 Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN
6 Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN
7 Department of Plant Physiology, University of Amsterdam, Swammerdam Institute for Life Sciences, Science Park 904, 1098 XH Amsterdam, The Netherlands
†Present address: Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN
§ Present address: Plant Biotechnology Division, National Institute of Biotechnology, Ganakbari, Savar, Dhaka 1349, Bangladesh
*Correspondence to: dudareva@purdue.edu
Plants synthesize an amazing diversity of volatile molecules important for reproduction and defense, serving as practical products for humans, and influencing atmospheric chemistry and climate. Despite progress on deciphering plant volatile biosynthesis, their release from the cell is poorly understood. The default assumption has been that volatiles passively diffuse out of cells. Here, characterization of Petunia hybrida adenosine triphosphate binding cassette (ABC) transporter, PhABCG1, demonstrates that passage of volatiles across the plasma membrane relies on active transport. PhABCG1-RNAi down-regulation results in decreased emission of volatiles, which accumulate to toxic levels in the plasma membrane. This study provides the first direct proof for a biologically-mediated mechanism of volatile emission.
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