Xylem vessel relays contribute to radial connectivity in grapevine stems (Vitis vinifera and V. arizonica

Authors: BRODERSON, CRAIG - University Of California; CHOAT, BRENDAN - Western Sydney University; CHATALET, DAVID - University Of Tennessee; SHACKEL, KENNETH - University Of California; MATTHEWS, MARK - University Of California; McElrone, Andrew

Submitted to: American Journal of Botany
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/19/2012
Publication Date: 1/23/2013
Citation: Broderson, C.R., Choat, B., Chatalet, D.S., Shackel, K.A., Matthews, M.A., Mcelrone, A.J. 2013. Xylem vessel relays contribute to radial connectivity in grapevine stems (Vitis vinifera and V. arizonica. American Journal of Botany. 100(2):314-321.

Interpretive Summary: Connectivity within xylem networks plays an important role in the movement of water and nutrients through plants, but also facilitates the spread of pathogens and embolisms that increase hydraulic resistance. This study describes a unique anatomical feature found in grapevine xylem that forms radial and tangential connections between spatially discrete vessels. We used High Resolution Computed Tomography, light microscopy, scanning electron microscopy (SEM), and single vessel dye injections to explore and describe the structure and function of peripheral xylem chains (PXCs) found to link non-adjacent vessels in stems of two Vitis species. PXCs were composed of 1-8 narrow diameter conduits (~25 µm), and were categorized as either short (477 µm mean axial length, which was approximately the same length of an average vessel element) or long (1774 µm mean axial length). Long PXCs accounted for 78% of the total, were composed of cells that partially overlapped along their axes for 100-500 µm, and usually spanned >2 vessel elements. The vast majority of PXCs in both V. vinifera and V. arizonica were oriented radially, connecting vessels within a sector delineated by rays. SEM analysis revealed scalariform pitting in shared cell walls located between vessels and PXC cells. The majority (67%) of V. vinifera PXCs lacked pit membranes entirely, and the remainder had either torn or remnants of pit membranes. Conversely, 93% of V. arizonica PXCs had intact pit membranes in at least one of the shared walls along the chain. The functional connectedness of vessels linked by PXCs was confirmed with single vessel dye injections. The PXCs described here likely play an important role in the known differential resistance of these grapevine species to systemic movement of vascular pathogens and drought-induced embolism.

Technical Abstract: Connectivity within xylem networks plays an important role in the movement of water and nutrients through plants, but also facilitates the spread of pathogens and embolisms that increase hydraulic resistance. This study describes a unique anatomical feature found in grapevine xylem that forms radial and tangential connections between spatially discrete vessels. We used High Resolution Computed Tomography, light microscopy, scanning electron microscopy (SEM), and single vessel dye injections to explore and describe the structure and function of peripheral xylem chains (PXCs) found to link non-adjacent vessels in stems of two Vitis species. PXCs were composed of 1-8 narrow diameter conduits (~25 µm), and were categorized as either short (477 µm mean axial length, which was approximately the same length of an average vessel element) or long (1774 µm mean axial length). Long PXCs accounted for 78% of the total, were composed of cells that partially overlapped along their axes for 100-500 µm, and usually spanned >2 vessel elements. The vast majority of PXCs in both V. vinifera and V. arizonica were oriented radially, connecting vessels within a sector delineated by rays. SEM analysis revealed scalariform pitting in shared cell walls located between vessels and PXC cells. The majority (67%) of V. vinifera PXCs lacked pit membranes entirely, and the remainder had either torn or remnants of pit membranes. Conversely, 93% of V. arizonica PXCs had intact pit membranes in at least one of the shared walls along the chain. The functional connectedness of vessels linked by PXCs was confirmed with single vessel dye injections. The PXCs described here likely play an important role in the known differential resistance of these grapevine species to systemic movement of vascular pathogens and drought-induced embolism.