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 ) asXstem ∝ H 1.52 andXstem ∝ LA 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 leaf ∝ MLA 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.