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The Functional Implications of Tracheary Connections Across BList1=SubBList1=BList1=SubBList BList1=SubBList3=BList1=SubBList2 Annals of Botany XX: 1–10, 2019 SubBList1=SubSubBList3=SubBList1=SubSubBList2 doi: 10.1093/aob/mcz076, available online at www.academic.oup.com/aob SubSubBList3=SubBList=SubSubBList=SubBList SubSubBList2=SubBList=SubSubBList=SubBList SubBList2=BList=SubBList=BList Keywords=Keywords=Keywords_First=Keywords The functional implications of tracheary connections across growth rings in four Keywords=HeadA=Keywords_Last=HeadA northern hardwood trees Downloaded from https://academic.oup.com/aob/advance-article-abstract/doi/10.1093/aob/mcz076/5537005 by Bates College user on 19 August 2019 HeadA=HeadB=HeadA=HeadB/HeadA Jay W. Wason1,2,*, Craig R. Brodersen2 and Brett A. Huggett3 HeadB=HeadC=HeadB=HeadC/HeadB HeadC=HeadD=HeadC=HeadD/HeadC 1School of Forest Resources, University of Maine, Orono, ME, USA, 2School of Forestry and Environmental Studies, Yale Extract3=HeadA=Extract1=HeadA University, New Haven, CT, USA and 3Department of Biology, Bates College, Lewiston, ME, USA CORI_HeadA=CORI_HeadB=CORI_HeadA=CORI_HeadB/HeadA *For correspondence. E-mail [email protected] CORI_HeadB=CORI_HeadC=CORI_HeadB=CORI_HeadC/HeadB Received: 4 January 2019 Returned for revision: 18 March 2019 Editorial decision: 30 April 2019 Accepted: 2 May 2019 CORI_HeadC=CORI_HeadD=CORI_HeadC=CORI_HeadD/HeadC CORI_Extract3=CORI_HeadA=CORI_Extract1=CORI_HeadA • Background and aims Deciduous angiosperm trees transport xylem sap through trunks and branches in ves- sels within annual growth rings. Utilizing previous growth rings for sap transport could increase vessel network ERR_HeadA=ERR_HeadB=ERR_HeadA=ERR_HeadB/HeadA size and redundancy but may expose new xylem to residual air embolisms in the network. Despite the important ERR_HeadB=ERR_HeadC=ERR_HeadB=ERR_HeadC/HeadB role of vessel networks in sap transport and drought resistance, our understanding of cross-ring connections within and between species is limited. ERR_HeadC=ERR_HeadD=ERR_HeadC=ERR_HeadD/HeadC • Methods We studied cross-ring connections in four temperate deciduous trees using dye staining and X-ray ERR_Extract3=ERR_HeadA=ERR_Extract1=ERR_HeadA microcomputed tomography (microCT) to detect xylem connectivity across growth rings and quantify their impact on hydraulic conductivity. SectionTitle=SectionTitle=SectionTitle=SectionTitle1 • Key results Acer rubrum and Fraxinus americana had cross-ring connections visible in microCT but only App_Head=App_HeadA=App_Head=App_HeadA/App_Head A. rubrum used previous growth rings for axial sap flow. Fagus grandifolia and Quercus rubra, however, did not HeadB=Text=HeadB=TextInd have cross-ring connections. Accounting for the number of growth rings that function for axial transport improved hydraulic conductivity estimates. • Conclusions These data suggest that the presence of cross-ring connections may help explain aspects of whole- tree xylem sap transport and should be considered for plant hydraulics measurements in these species and others with similar anatomy. Key words: Acer rubrum, connectivity, diffuse porous, earlywood, Fagus grandifolia, Fraxinus americana, growth rings, hydraulics, latewood, Quercus rubra, ring porous, xylem. INTRODUCTION experiments (Melcher et al., 2003; Nolf et al., 2017), all sug- gesting that in some species xylem sap can flow across annual Deciduous angiosperm trees transport xylem sap through growth ring boundaries. the trunk and branches in networks of conduits formed in an- Recruiting previous growth rings for axial xylem sap trans- nual growth rings. Within a growth ring, most axial xylem sap port via cross-ring connections would increase the total number transport occurs in vessels because of their large diameter, of functional xylem conduits, thereby increasing both network and therefore lower resistance, relative to fibres and tracheids. redundancy (Loepfe et al., 2007) and the ‘return’ on the initial Xylem within the trunk is often divided into two categories: investment in past xylem production. In all species, cross-ring the older, non-functional heartwood and the younger, func- connections between growth rings allow older xylem to serve as tional sapwood. Sapwood is typically composed of several a large capacitive reservoir to buffer the xylem sap from reaching annual growth rings, with the majority of xylem sap flowing excessively negative water potentials (Tyree and Zimmermann, axially through the current-year xylem (Ellmore and Ewers, 2002; Borchert and Pockman, 2005; Fukuda et al., 2015; 1986; Melcher et al., 2003), but the contribution of previously Matheny et al., 2015). Cross-ring connections could also expand formed growth rings is variable among species and wood types the xylem vessel network and allow multiple growth rings to (Phillips et al., 1996; Umebayashi et al., 2008; Berdanier contribute to axial flow (Fig. 1A). However, because deciduous et al., 2016). Partitioning the total axial xylem sap flux into leaves are connected to the current-year xylem, the lowest- the relative contributions of each growth ring is difficult be- resistance pathway for axial xylem sap transport would usually cause of the spatial resolution of standard sap flow sensors be through the current annual ring. Therefore, the previous-year compared with the width of annual rings and uncertainty about rings likely contribute to axial flow if there is high evaporative which rings are being measured (Granier et al., 1994; Phillips demand, if the current-year xylem becomes dysfunctional from et al., 1996; Bush et al., 2010; Berdanier et al., 2016). Studies embolism or damage (Fig. 1B), or if there are partial or ‘missing’ have addressed this issue with sap flow sensors installed at dif- growth rings (Lorimer et al., 1999). If the current-year xylem ferent depths (Phillips et al., 1996; Gebauer et al., 2008; Bush becomes dysfunctional, xylem sap would need to move radi- et al., 2010; Berdanier et al., 2016), dye tracing (Ellmore and ally from the previous rings into the current-year xylem before Ewers 1986; Umebayashi et al., 2008, 2010) and hydraulics © The Author(s) 2019. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: [email protected]. 2 Wason et al. — Cross-ring xylem connections A B EW LW EW LW EW LW EW LW EW LW EW LW LW EW Downloaded from https://academic.oup.com/aob/advance-article-abstract/doi/10.1093/aob/mcz076/5537005 by Bates College user on 19 August 2019 Embolism 2016 2017 2018 2016 2017 2018 C D EW LW EW LW EW LW EW LW EW LW EW LW 2016 2017 2018 2016 2017 2018 Fig. 1. Diagrammatic representation of some potential radial pathways for xylem sap and embolism movement between annual rings. In (A), the boundary be- tween latewood (LW) and earlywood (EW) of subsequent years with inter-conduit connections (vertical dashed lines) allows significant contributions of previous growth rings to the axial bulk flow. Radial flow encounters resistance (horizontal resistor symbols), which can be divided into two categories [transverse view of two conduits shown in the inset in (A)]: low-resistance flow via pits (solid arrows) between xylem conduits (circles) and high-resistance flow through the cell walls (dashed arrow). In (B), an embolism (vertical resistor symbol) arising in the current-year ring (2018) blocks axial flow, but radial connectivity allows alternative pathways around the blockage but with increased resistance (dashed arrow in B). In (C), residual embolism in previous year xylem (2017) can follow the same radial inter-conduit pathways via pit membrane connections. In (D), species without direct connections via pits across the growth ring boundary (vertical solid lines) can isolate the spread of residual embolism to current-year xylem but the lack of cross-ring pitting results in very high resistance pathways for axial and radial contributions from older xylem [narrower curved arrows than in (A–C)]. it could enter the transpiration stream (Fig. 1B), either through could isolate residual embolisms to previous growth rings lower-resistance direct intervessel connections or by diffusion (Choat et al., 2015), thereby protecting the current-year growth through higher-resistance cell walls. from the legacy effects of past drought or frost (Fig. 1D). It is Embolism formation resulting from exposure to drought or therefore important to determine the extent of cross-ring con- freeze–thaw events (Sperry and Sullivan, 1992) can lead to hy- nections among species and their potential impact on xylem draulic dysfunction. A larger interconnected multi-year xylem network organization and sap transport (Umebayashi et al., network would increase the number of alternative pathways for 2008). xylem sap transport (Ellmore et al., 2006). However, an inter- Identifying the specific pathway through which xylem sap connected multi-year xylem network could also be a liability travels across the latewood–earlywood boundary between two (Loepfe et al., 2007), as residual emboli, unless blocked by adjacent annual rings is critical for determining the resistance tyloses or gums (Cochard and Tyree, 1990), could spread to the to radial xylem sap movement. Efficient radial flow of xylem current-year xylem through the same cross-ring connections sap across growth ring boundaries likely occurs through low- (Fig. 1C). Alternatively, the absence of cross-ring connections resistance pit membrane connections within pit fields between Wason et al. — Cross-ring xylem connections 3 neighbouring cells (Tyree
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