References
Anfodillo T., Carraro V., Carrer M., Fior C. & Rossi S. (2006) Convergent tapering of xylem conduits in different woody species.New Phytol , 169 , 279-290.
Banavar J.R., Cooke T.J., Rinaldo A. & Maritan A. (2014) Form, function, and evolution of living organisms. Proceedings of the National Academy of Sciences , 111 , 3332-3337.
Blonder B., Violle C., Bentley L.P. & Enquist B.J. (2011) Venation networks and the origin of the leaf economics spectrum. Ecology Letters , 14 , 91-100.
Boer H.J., Price C.A., Wagner-Cremer F., Dekker S.C., Franks P.J. & Veneklaas E.J. (2016) Optimal allocation of leaf epidermal area for gas exchange. New Phytologist , 210 , 1219-1228.
Brodribb T.J., McAdam S.A. & Carins Murphy M.R. (2017) Xylem and stomata, coordinated through time and space. Plant Cell and Environment , 40 , 872-880.
Cai J. & Tyree M.T. (2010) The impact of vessel size on vulnerability curves: data and models for within‐species variability in saplings of aspen, Populus tremuloides Michx. Plant, Cell & Environment ,33 , 1059-1069.
Carins Murphy M.R., Jordan G.J. & Brodribb T.J. (2014) Acclimation to humidity modifies the link between leaf size and the density of veins and stomata. Plant, Cell & Environment , 37 , 124-131.
Carins Murphy M.R., Jordan G.J. & Brodribb T.J. (2016) Cell expansion not cell differentiation predominantly co-ordinates veins and stomata within and among herbs and woody angiosperms grown under sun and shade.Annals of Botany , 118 , 1127-1138.
Castro-Díez P., Puyravaud J.P. & Cornelissen J.H.C. (2000) Leaf structure and anatomy as related to leaf mass per area variation in seedlings of a wide range of woody plant species and types.Oecologia , 124 , 476-486.
Castro-Díez P., Puyravaud J.P., Cornelissen J.H.C. & Villar-Salvador P. (1998) Stem anatomy and relative growth rate in seedlings of a wide range of woody plant species and types. Oecologia , 116 , 57-66.
Cornelissen J.H.C., Castro-Díez P. & Hunt R. (1996) Seedling growth, allocation and leaf attributes in a wide range of woody plant species and types. Journal of Ecology , 84 , 755-765.
Cornelissen J.H.C., Cerabolini B., Castro-Diez P., Villar-Salvador P., Montserrat-Marti G., Puyravaud J.P., Maestro M., Werger M.J.A. & Aerts R. (2003a) Functional traits of woody plants: correspondence of species rankings between field adults and laboratory-grown seedlings?Journal of Vegetation Science , 14 , 311-322.
Cornelissen J.H.C., Cerabolini B., Castro-Díez P., Villar-Salvador P., Montserrat-Martí G., Puyravaud J.P., Maestro M., Werger M.J.A. & Aerts R. (2003b) Functional traits of woody plants: correspondence of species rankings between field adults and laboratory-grown seedlings?Journal of Vegetation Science , 14 , 311-322.
Echeverría A., Anfodillo T., Soriano D., Rosell J.A. & Olson M.E. (2019) Constant theoretical conductance via changes in vessel diameter and number with height growth in Moringa oleifera. Journal of Experimental Botany .
Enquist B.J. (2002) Universal scaling in tree and vascular plant allometry: toward a general quantitative theory linking plant form and function from cells to ecosystems. Tree Physiology , 22 , 1045-1064.
Fiorin L., Brodribb T.J. & Anfodillo T. (2016) Transport efficiency through uniformity: organization of veins and stomata in angiosperm leaves. New Phytologist , 209 , 216-227.
Franks P.J. & Farquhar G.D. (2007) The mechanical diversity of stomata and its significance in gas-exchange control. Plant Physiology ,143 , 78-87.
Hendry G.A.F. & Grime J.P. (1993) Methods in comparative plant ecology : a laboratory manual . Chapman & Hall, London.
Jacobsen A.L., Pratt R.B., Venturas M.D. & Hacke U.G. (2019) Large volume vessels are vulnerable to water-stress-induced embolism in stems of poplar. Iawa Journal , 40 , 4-S4.
Lechthaler S., Colangeli P., Gazzabin M. & Anfodillo T. (2019) Axial anatomy of the leaf midrib provides new insights into the hydraulic architecture and cavitation patterns of Acer pseudoplatanus leaves.Journal of Experimental Botany , 70 , 6195-6201.
Li Y., Reich P.B., Schmid B., Shrestha N., Feng X., Lyu T., Maitner B.S., Xu X., Li Y. & Zou D. (2020) Leaf size of woody dicots predicts ecosystem primary productivity. Ecology Letters .
Liu H., Gleason S.M., Hao G., Hua L., He P., Goldstein G. & Ye Q. (2019) Hydraulic traits are coordinated with maximum plant height at the global scale. Science Advances , 5 , eaav1332.
Meinzer F. & Grantz D. (1990) Stomatal and hydraulic conductance in growing sugarcane: stomatal adjustment to water transport capacity.Plant, Cell & Environment , 13 , 383-388.
Meinzer F.C. (2002) Co‐ordination of vapour and liquid phase water transport properties in plants. Plant, Cell & Environment ,25 , 265-274.
Olson M.E., Anfodillo T., Rosell J.A., Petit G., Crivellaro A., Isnard S., León‐Gómez C., Alvarado‐Cárdenas L.O. & Castorena M. (2014) Universal hydraulics of the flowering plants: vessel diameter scales with stem length across angiosperm lineages, habits and climates.Ecology Letters , 17 , 988-997.
Parlange J.-Y. & Waggoner P.E. (1970) Stomatal dimensions and resistance to diffusion. Plant Physiology , 46 , 337-342.
Roddy A.B., Théroux-Rancourt G., Abbo T., Benedetti J.W., Brodersen C.R., Castro M., Castro S., Gilbride A.B., Jensen B. & Jiang G.-F. (2020) The scaling of genome size and cell size limits maximum rates of photosynthesis with implications for ecological strategies.International Journal of Plant Sciences , 181 , 75-87.
Rosell J.A. & Olson M.E. (2019) To furcate or not to furcate: the dance between vessel number and diameter in leaves. Journal of Experimental Botany , 70 , 5990-5993.
Sack L., Dietrich E.M., Streeter C.M., Sanchez-Gomez D. & Holbrook N.M. (2008) Leaf palmate venation and vascular redundancy confer tolerance of hydraulic disruption. Proc Natl Acad Sci U S A , 105 , 1567-1572.
Sack L., Scoffoni C., McKown A.D., Frole K., Rawls M., Havran J.C., Tran H. & Tran T. (2012) Developmentally based scaling of leaf venation architecture explains global ecological patterns. Nature Communications , 3 , 837.
Sevanto S., Holbrook N.M. & Ball M.C. (2012) Freeze/Thaw-induced embolism: probability of critical bubble formation depends on speed of ice formation. Frontiers in Plant Science , 3 , 107-107.
Shinozaki K., Yoda K., Hozumi K. & Kira T. (1964) A quantitative analysis of plant form-the pipe model theory: I. Basic analyses.Japanese Journal of Ecology , 14 , 97-105.
Simonin K.A. & Roddy A.B. (2018) Genome downsizing, physiological novelty, and the global dominance of flowering plants. Plos Biology , 16 , e2003706.
Sterck F. & Zweifel R. (2016) Trees maintain a similar conductance per leaf area through integrated responses in growth, allocation, architecture and anatomy. Tree Physiology , 36 , 1307-1309.
Team R.D.C. (2014) R: a language andenvironment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. http:// www.R-project.org/.
West G.B., Brown J.H. & Enquist B.J. (1999) A general model for the structure and allometry of plant vascular systems. Nature ,400 , 664-667.
Zanne A.E., Tank D.C., Cornwell W.K., Eastman J.M., Smith S.A., FitzJohn R.G., McGlinn D.J., O’Meara B.C., Moles A.T., Reich P.B., Royer D.L., Soltis D.E., Stevens P.F., Westoby M., Wright I.J., Aarssen L., Bertin R.I., Calaminus A., Govaerts R., Hemmings F., Leishman M.R., Oleksyn J., Soltis P.S., Swenson N.G., Warman L. & Beaulieu J.M. (2014) Three keys to the radiation of angiosperms into freezing environments.Nature , 506 , 89-92.
Zhang F.P., Carins Murphy M.R., Cardoso A.A., Jordan G.J. & Brodribb T.J. (2018) Similar geometric rules govern the distribution of veins and stomata in petals, sepals and leaves. New Phytologist ,219 , 1224-1234.
Zhong M., Castro-Diez P., Puyravaud J.P., Sterck F.J. & Cornelissen J.H.C. (2019) Convergent xylem widening among organs across diverse woody seedlings. New Phytol , 222 , 1873-1882.
Fig.1 Conceptual framework of this research concerning allometric relations of plant hydraulics across woody species. Natural selection acts on heritable variation between individuals within the same species. Individuals with vessels that do not widen with height growth, or widen little, will experience continual declines in leaf-specific conductance with height growth and therefore declining growth and reproductive output per unit leaf area. Individuals with vessels that widen very markedly would have conduits of low resistance, in contrast to the high-resistance variants with conduits that are ‘too narrow’, but they would have their own set of disadvantages. For example, for a given leaf area and transpirational demand, the wider conduits cost more for the same service provided. Each unit of carbon invested in excessively wide vessels is a unit that is not invested in further growth or reproduction, and so these variants should be at a selective disadvantage (Banavar, Cooke, Rinaldo & Maritan, 2014). Moreover, wider vessels are more vulnerable to gas embolisms that obstruct conductance, both from freezing ((Sevanto, Holbrook & Ball, 2012, Zanne, Tank, Cornwell, Eastman, Smith, FitzJohn, McGlinn, O’Meara, Moles, Reich, Royer, Soltis, Stevens, Westoby, Wright, Aarssen, Bertin, Calaminus, Govaerts, Hemmings, Leishman, Oleksyn, Soltis, Swenson, Warman & Beaulieu, 2014) and likely drought as well (Cai & Tyree, 2010, Jacobsen, Pratt, Venturas & Hacke, 2019, Liu, Gleason, Hao, Hua, He, Goldstein & Ye, 2019). As a result, plants with vessels that are ‘too wide’ would also be at a selective disadvantage (Zhong et al. (2019)). The variants that should have the largest amounts of surplus carbon to devote to growth and reproduction are those in the intermediate zone, in which conduits widen just enough that conductance remains constant per unit leaf area, but not so much as to incur excessive carbon costs and embolism vulnerability.
In our previous study, based on the same woody seedling populations, we found that, at the whole-plant level, the stem xylem cross-sectional area (Xstem ) of stem medium (a) closely scales with stem height (H ) and total leaf area per plant (LA ) asXstemH 1.52 andXstemLA 0.75 across all the studied species. For individual leaves, vessel diameter (D leaf) in the medium of leaf midvein (b) closely scales with average leaf area (MLA ) asD leafMLA 0.21 (Zhonget al. (2019). In this study, we test the poorly understood xylem-stomata covariation from the size perspective We ask: are there scaling relationships between total stomatal area and xylem cross-sectional area across species, at the entire plant and at individual leaf level? Specifically, we zoom in on the terminal part of water exchange (from minor vessels to stomata), and ask: does the minor vessel number (which scales with leaf area; see (Lechthaler et al. , 2019, Rosell & Olson, 2019)) scale with stomatal number per leaf and per plant across these woody seedlings? The conceptual picture should deepen our understanding of plants’ water transport system and have broad implications for integrating xylem architecture and stomatal distribution.Fig. 2 Size-covariation of stomata and xylem at the whole plant level, across seedlings of 53 European woody species varying in leaf-habit, growth-form and relative growth rate (RGR). (a) Convergent scaling of plant total stomatal area and stem xylem transect area. (b) Convergent scaling of plant total stomatal area and stem xylem conductance area. Lines indicate significant scaling relationships. Growth forms: T tree, S shrub, SS subshrub,C+Sc scrambler or climber. Regression coefficients of standardized major axis (SMA) are documented in Table 1.
Fig. 2 Size-covariation of stomata and xylem at the whole plant level, across seedlings of 53 European woody species varying in leaf-habit, growth-form and relative growth rate (RGR). (a) Convergent scaling of plant total stomatal area and stem xylem transect area. (b) Convergent scaling of plant total stomatal area and stem xylem conductance area. Growth forms: T tree, S shrub, SS subshrub,C+Sc scrambler or climber. Regression coefficients of standardized major axis (SMA) are documented in Table 1.
Fig. 3 Convergent scaling of leaf total stomatal area and midvein xylem transect area, across seedlings of 53 European woody species varying in leaf-habit, growth-form and relative growth rate (RGR). Lines indicate significant scaling relationships. Growth forms: T tree, Sshrub, SS subshrub, C+Sc scrambler or climber. Regression coefficients of standardized major axis (SMA) are documented in Table 1.
Fig. 4 (a) Covariation of leaf total stomatal number and midvein xylem area (or average leaf area, insert). (b) Relationship between average stomatal area and midvein xylem area (or average leaf area, insert). (c) Covariation of plant total stomatal number and stem xylem area (or total leaf area, insert). (d) Relationship between minor vessel area and stem xylem area (or total leaf area, insert). Lines indicate significant scaling relationships. Growth forms: T tree, S shrub,SS subshrub, C+Sc scrambler or climber. Regression coefficients of standardized major axis (SMA) are documented in Table 1.
Fig. 5 (a) Covariation of plant total stomatal number and plant minor vessel number. (b) Relation between average stomatal area and average minor vessel area. Lines indicate significant scaling relationships. Growth forms: T tree, S shrub, SS subshrub,C+Sc scrambler or climber. Regression coefficients of standardized major axis (SMA) are documented in Table 1.
Table 1. Ln – Ln scaling relationships were analyzed with standardized major axis regression (SMA) analyses, with additional reference to the contributions of different growth forms, leaf habits and relative growth rates (RGRs) to these relationships. Y-intercept and slopes as well as slope homogeneity with 1 are reported for pairwise relationships with significant results. 95% confidence intervals (CI) are in parentheses. Growth-form: T tree, S shrub, SS subshrub,C+Sc scrambler or climber; Leaf-habit: D deciduous,E evergreen. Y/X – RGR SMA regression of Y/X (ratio of Y values to X values) and RGR. ***, P < 0.001; **P < 0.05; ns, not significant.