Skip to main content
NCBI home page
Wiley Open Access Collection logoLink to Wiley Open Access Collection
. 2025 Aug 12;248(2):628–636. doi: 10.1111/nph.70467

Tip‐to‐base conduit widening maintains hydraulic efficiency in aerial fern organs

Yuliia Khoma 1,2, Scott A M McAdam 1,✉
PMCID: PMC12445813  PMID: 40798993

Summary

  • Tip‐to‐base conduit widening is critical for hydraulic efficiency; yet few studies have investigated the full developmental potential of xylem.

  • We utilized the diverse growth habits of ferns to test whether a wide developmental potential of xylem is constrained by growth habit. We documented xylem hydraulically weighted conduit diameter (Dh) across the vertical stem of the tall Equisetum giganteum L.; in the soil surface rhizome that roots at each node of Phlebodium pseudoaureum (Cav.) Lellinger and its vertical leaf. In addition, we determined Dh across aquatic and aerially suspended rhizomes of Marsilea hirsuta L.

  • Considerable tip‐to‐base conduit widening was observed in the stems of E. giganteum, aerially‐suspended rhizomes of M. hirsuta, and the vertical leaves of P. pseudoaureum, organs in which selection would favor the maintenance of hydraulic efficiency toward the apex. No change in Dh was observed along the soil‐surface rhizomes of P. pseudoaureum or the aquatic rhizomes of M. hirsuta.

  • Our results indicate that there is considerable developmental potential for xylem conduit diameter in ferns apparent under conditions in which hydraulic efficiency is not required for survival; but that tip‐to‐base conduit widening is consistently observed in fern organs that require an efficient long‐distance transport of water to the apex.

Keywords: fern, hydraulic diameter (Dh), tapering, turgor, water potential, xylem

Introduction

Vascular plants efficiently transport water and dissolved nutrients from the roots to other organs using a specialized tissue called xylem. Being largely comprised of dead sclerenchyma cells, xylem provides a low resistance transport path for water, which is relatively resistant to embolism formation and provides mechanical strength (Baas et al., 2004; Chave et al., 2009; Brodribb & Mencuccini, 2017). The morphological characteristics of xylem elements have considerable influence over water transport efficiency and safety. Of particularly note, across the stems of terrestrial plants, xylem anatomy varies in a highly consistent way, with conduits widening from tip‐to‐base, sometimes this phenomenon is also referred to as conduit tapering (Sanio, 1872; Rosell et al., 2017; Lechthaler et al., 2020; Olson et al., 2021; Chambers‐Ostler et al., 2023). This near‐universal observation has important adaptive explanations (Petit, 2024). It has been proposed that as plants grow taller, the diameter of the distal xylem vessels must increase to reduce the resistance to water flow and improve the efficiency of water transport throughout the plant (West et al., 1997; Olson & Arroyo‐Santos, 2015; Koçillari et al., 2021).

The observation of tip‐to‐base conduit widening across a wide diversity of terrestrial plant species, following a power‐function with an exponent of c. 0.2, suggests this trait is under strong selection (West et al., 1999; Becker et al., 2000; Anfodillo et al., 2006; Koçillari et al., 2021; Bok et al., 2022). Tip‐to‐base conduit widening as an adaptation, favored by selection, is currently the best‐supported model explaining this trait because of the need to maintain conductance as the conductive pathlength and hydraulic resistance increases (Olson et al., 2021; Rodriguez‐Zaccaro et al., 2021). Evidence supporting a strong selective pressure driving a consistent developmental tip‐to‐base widening of conduits arises from studies at the population level (Rodriguez‐Zaccaro et al., 2021), interspecific comparisons (Olson et al., 2018, 2021), and optimality modeling (West et al., 1999; Petit & Anfodillo, 2009; Savage et al., 2010; Couvreur et al., 2018; Koçillari et al., 2021).

A less‐likely alternative, given how common optimality models predict tip‐to‐base conduit widening across the diversity of land plants, is the hypothesis that the widening of xylem conduit diameter away from the apex is really a tapering towards the apex that is driven by hydraulic constraints on plant development (Cabon et al., 2020). High turgor pressure is required for cell expansion, which may affect the diameter of xylem cells. Given the gradient in water potential across a stem from the soil to the sites of evaporation in the leaf, there is a natural gradient in water status and turgor pressure along a stem, which might result in reduced developmental expansion of vessels (Ray & Green, 1972; Hacke et al., 2006; Cabon et al., 2020). If passive cell expansion, driven by turgor, is the primary mechanism for conduit tapering, then it is less likely that this phenomenon is under active selection for increased efficiency in water transport. Instead, it could simply be a function of plant water status during cell expansion. Consequently, factors such as drought, high temperature, or increased evaporative demand might influence the extent of conduit tapering (Sperry et al., 2002; Tyree & Zimmermann, 2002; Sack & Holbrook, 2006; Meinzer et al., 2010; Anfodillo et al., 2012; Lens et al., 2013; Rosell & Olson, 2014).

Most data to date documenting xylem tip‐to‐base conduit widening derives from terrestrial plants in which strong selection should be driving a consistent exponential relationship between conduit diameter and proximity to stem apex (Koçillari et al., 2021). We do not know if selection for tip‐to‐base conduit widening is relaxed under aquatic conditions, or conditions in which there is no gradient of water status along the stem. Drobnitch et al. (2015) have shown that there is phloem conduit tapering in kelp, suggesting that similar tip‐to‐base conduit scaling might occur in all plants, not just terrestrial species.

We hypothesized that given the observations of tip‐to‐base conduit widening across terrestrial plants (Anfodillo et al., 2006; Olson et al., 2014; Koçillari et al., 2021; Bok et al., 2022), we would observe this phenomenon broadly across ferns. The structure of xylem in ferns differs significantly from most seed plants, as it is comprised of primary xylem, which does not undergo secondary growth (Suissa & Friedman, 2021). The primary elements of the xylem in most species of ferns are tracheids (Mahley et al., 2018), which are elongated cells with thickened lignified walls, but vessels have been reported in a number of groups, including the genus Marsilea (Schneider & Carlquist, 2000b). Given the primary nature of fern xylem, it is consequently established early in stem development (Bierhorst, 1960; White, 1963; Carlquist & Schneider, 2001). Another feature of ferns as a group is that there is considerable diversity in stem morphology and growth habit, from near‐arborescent species with erect stems (Smith et al., 2008) to terrestrial and epiphytic species that have rhizomes in contact with the substrate, to aquatic and semi‐aquatic species that can have rhizomes that grow in and out of water (Smith et al., 2008; Westbrook & McAdam, 2021). Despite this diversity and the long evolutionary history and ecological breadth of this group of land plants, little is known about the vascular properties of xylem of ferns (Pittermann et al., 2013; Suissa & Friedman, 2021).

Here we use the diversity of fern stem morphologies to specifically investigate whether tip‐to‐base conduit widening is under selection in this group. Koçillari et al. (2021) have previously observed tip‐to‐base conduit widening in the vertical stems of 5.3 m tall Equisetum myriochaetum Schltdl. & Cham. and Selaginella and Lycopodium, as well as in the leaves of Lophosoria quadripinnata (J.F.Gmel.) C.Chr. We hypothesize that when stems or leaves of ferns are grown under conditions that require the development of an efficient water transport system, such as in erect aerial stems, rhizomes growing suspended in air out of water or across large leaves, then tip‐to‐base conduit widening will be observed (Koçillari et al., 2021; Olson et al., 2021). By contrast, when stems are grown under conditions in which there is no environmental pressure to maintain tip‐to‐base conduit widening for hydraulic efficiency, like in prostrate rhizomes that root at each node or in submerged aquatic rhizomes, then alternative conduit scaling functions from tip‐to‐base may manifest.

Materials and Methods

Plant material and growth conditions

We chose three species of fern (Marsilea hirsuta L., Equisetum giganteum L. and Phlebodium pseudoaureum (Cav.) Lellinger) that have highly divergent stem or rhizome morphology and habit. Plants were grown in the Lilly glasshouses at Purdue University (West Lafayette, IN, USA).

Marsilea hirsuta belongs to a small family of semi‐aquatic ferns, Marsileaceae. Marsilea species have a number of highly divergent reproductive, physiological, and ecological traits compared to other fern groups (Schneider & Pryer, 2002; Westbrook & McAdam, 2021). Marsilea hirsuta has a rhizome capable of transitioning between aquatic and terrestrial environments (Westbrook & McAdam, 2021). The rhizomes are typically slender and creeping, allowing the plant to root both underwater and in moist ground. They have compound leaves with four leaflets that are highly responsive to environmental signals, possessing nyctinasty (daily movement of leaflet orientation), a trait not found in other fern groups (Vasco et al., 2013). Plants of M. hirsuta were grown in flooded tubs on a bench. The tubs were half‐filled with topsoil; plants were allowed to grow to fill the tub, and rhizomes were allowed to extend and grow over the edge of the tub so that they became suspended in air.

Equisetum giganteum is a giant horsetail, one of the largest living members of this group of ferns (Husby, 2009). Equisetum giganteum has a hollow upright stem, reinforced by nodal thickenings and septa, and can grow to over 5 m in height. The relatively small diameters of E. giganteum stems (< 4 cm) pose a mechanical stability challenge against buckling (Husby, 2009).

Phlebodium pseudoaureum is a terrestrial or epiphytic fern that has large glaucous fronds (up to 1 m in length) originating from a broad, trichome‐covered, prostrate rhizome that clings to the soil surface and roots at each node (Tejero‐Díez et al., 2009). Mature individuals of E. giganteum and P. pseudoaureum were grown in in‐ground beds in the glasshouse with no restriction on growth space or light.

Sample preparation and anatomical measurements

Three rhizomes, stems, or leaves were selected for each fern species or growth type in M. hirsuta. Distance from the apex was measured in all. Transverse sections along the rhizomes of M. hirsuta were made every 1 cm from the apex for 35–40 cm. In P. pseudoaureum, transverse sections of the rhizome from the apex were made every 10 cm for 40 cm, as well as across a frond from leaf tip to base at the node. Since the length of the stem in E. giganteum exceeded 2 m, we made transverse sections along the length of the stem every 40 cm; we found that xylem had not fully developed and matured in the upper 40 cm of the tall stems. Conduit data collected in this cell differentiation and elongation region was not used to determine conduit scaling relationships. Cross‐sections (20–30 μm thick) were prepared using a freezing microtome (Microm HM 430; Thermo Scientific, Waltham, MA, USA). Sections were stained with aqueous toluidine blue (0.1% in H2O) before being mounted on a glass slide using glycerine jelly. Stained sections were examined using a fluorescence microscope (Zeiss Axio Scope) with an appropriate long pass filter for autofluorescence, and digital images of the xylem were taken under fluorescence at ×10 magnification for M. hirsuta and under visible light at ×10 magnification for rhizomes of P. pseudoaureum and at ×20 magnification for E. giganteum samples. Measurements of xylem conduit diameter were conducted using ImageJ (Schindelin et al., 2012).

Conduit diameter was calculated assuming the lumen to be circular. We chose conduits with a diameter of more than half the diameter of the largest conduit to eliminate those that may have been tapered ends, as suggested by James et al. (2003). Selected cells were averaged as the hydraulic diameter (Dh), so that cell diameters were weighted according to hydraulic conductance (Kolb & Sperry, 1999; Anfodillo et al., 2006):

Dh=∑dn5∑dn4

where d n is the diameter of the n cell (Sperry et al., 1994).

Water potential

Three leaves, or stem apices, from each species were collected from across the length of the rhizome (apex, middle and base‐ which we considered to be the end of the length along which conduit diameter was measured) along the rhizome of each fern sample for determination of mean midday leaf water potential (MPa) on a sunny day. Leaves were excised and wrapped in damp paper towel with no surface water and immediately placed into a humid plastic bag as per Rodriguez‐Dominguez et al. (2022). Midday leaf water potential was measured using a pressure chamber (PMS Instrument Co., Corvallis, OR, USA). Stem water potential was measured in E. giganteum by sampling shoots pre‐dawn from across the canopy.

Statistical analyses

Statistical analysis was performed according to common methods. Data are presented as the mean value ± SE. Differences between xylem hydraulic diameter measurements along the rhizome from tip to base and water potential were analyzed using a one‐way analysis of variance (ANOVA). Mean comparisons were performed using a post‐hoc pairwise Tukey's test. All tests were declared significant at P < 0.05. Statistical analyses were performed in the SPSS 29.0 Software (IBM, Inc., NY, USA).

Results

Anatomical measurements

Mean hydraulic diameter of xylem conduits (Dh) along the leaf, rhizome, or stem varied across the three species of ferns examined (Table 1). M. hirsuta had the narrowest conduit diameter of all species measured, with stems growing in water having a mean Dh of c. 54.03 ± 2.27 μm (Table 1). In E. giganteum, the largest mean Dh was 62.77 ± 0.43 μm at the base of the stem (Table 1). In P. pseudoaureum, the largest mean Dh was 85.34 ± 1.79 μm measured in the rhizome, with the mean Dh at the base of the stipe being 76.13 ± 9.48 μm narrowing to 25.07 ± 4.51 μm in the midrib at the leaf apex (Table 1).

Table 1.

Average hydraulic diameter (Dh) of xylem from top to base in ferns rhizomes, stems or leaves.

Species Organ Distance from apex (cm) Dh (μm) ± SE Exponent
Marsilea hirsuta Aquatic rhizome 1 53.00 ± 1.73a 0
15 54.03 ± 2.27a
30 54.78 ± 2.03a
Marsilea hirsuta Aerially suspended rhizome 1 41.99 ± 1.27a 0.27
20 49.53 ± 1.83b
45 59.60 ± 2.46c
Equisetum giganteum Stem 1 35.22 ± 2.27a 0.34
75 46.82 ± 3.044b
200 62.77 ± 0.43c
Phlebodium pseudoaureum Rhizome 0 83.07 ± 3.33a 0
20 85.34 ± 1.79a
40 82.28 ± 2.18a
Phlebodium pseudoaureum Leaf 5 25.07 ± 4.51a 0.46
30 54.43 ± 12.66b
60 76.13 ± 9.48c
Open in a new tab

Different letters indicate significant differences in Dh across a rhizome or stem using a post‐hoc pairwise Tukey's test at P < 0.05. The exponents for two‐factor power functions fitted to Dh and distance from apex data are shown.

In M. hirsuta, Dh along aquatic, submerged rhizomes did not change from tip‐to‐base, with mean Dh varying between 53 and 55 μm along 30 cm of rhizome (Fig. 1a). By contrast, in rhizomes of this species that grew out of standing water and into air, we observed a considerable and significant reduction in Dh towards the apex in regions of the rhizome with mature and no longer differentiating xylem, with xylem maturation and full leaf expansion occurring at c. 17 cm from the apex (Fig. 2a). In the aerially suspended rhizomes of M. hirsuta growing out of water, Dh increased away from the tip (41.99 μm) to base (59.60 μm) (Table 1) 40 cm away from the apex. The rhizome bases were submerged in these aerially suspended stems. This tip‐to‐base widening followed a significant two‐parameter power function (R 2 = 0.81, P < 0.01) with an exponent of 0.27 (Fig. 2a; Table 1).

Fig. 1.

Fig. 1

Open in a new tab

No tip‐to‐base conduit widening in aquatic rhizomes of Marsilea hirsuta. (a) Mean hydraulically weighted xylem conduit diameter (Dh) along the rhizome of aquatic rhizomes of M. hirsuta (insert depicts an aquatic rhizome once water is drained away growing on substrate). Representative images of transverse sections of an aquatic rhizome of M. hirsuta (b) at the apex, (c) 15 cm from the apex, and (d) 30 cm from the apex. Sections were stained with aqueous toluidine blue, and images were taken at ×10 magnification under ultraviolet light with a long pass filter. The arrow in b shows the location of the xylem. Bars, 500 μm. Error bars show ±SE (n = 3).

Fig. 2.

Fig. 2

Open in a new tab

Tip‐to‐base conduit widening in aerially suspended rhizomes of Marsilea hirsuta. (a) Mean hydraulically weighted xylem conduit diameter (Dh) along aerially suspended rhizomes of M. hirsuta that grew away from standing water into air (insert depicts an aerially growing rhizome; bar denotes the region of the rhizome in which active xylem differentiation and maturation is occurring). A two‐parameter power function is fitted to data along the rhizome from when xylem maturation is complete; an R 2 for this function is shown. Representative images of transverse sections of an aerially suspended rhizome of M. hirsuta that grew away from standing water (b) at the apex, (c) 20 cm from the apex, and (d) 42 cm from the apex in close proximity to water. Sections were stained with aqueous toluidine blue, and images were taken at ×10 magnification under ultraviolet light with a long pass filter. The arrow in b shows the location of the xylem. Bars, 500 μm. Error bars show ±SE (n = 3). In aerially suspended rhizomes of M. hirsuta, the apex was the most distal tissue from the water, more distal than any leaf along the rhizome.

Anatomical measurements of the stem of E. giganteum revealed a significant difference in Dh relative to the distance from the stem apex (Fig. 3a). Dh almost doubled along the stem away from the apex, with Dh increasing from a mean of 35.22 ± 2.27 μm once xylem had finished differentiating at c. 40 cm from the apex to a mean of 62.77 ± 0.43 μm 200 cm along the stem (Table 1; Fig. 3a). The increase in Dh from the tip followed a significant two‐parameter power function (R 2 = 0.97, P < 0.001) with an exponent of 0.34 (Fig. 3a; Table 1).

Fig. 3.

Fig. 3

Open in a new tab

Tip‐to‐base conduit widening in vertical stems of Equisetum giganteum. (a) Mean hydraulically weighted xylem conduit diameter (Dh) along the vertical stems of E. giganteum (the insert depicts the stems of E. giganteum; bar denotes the region of the stem in which active xylem differentiation and maturation is occurring). A two‐parameter power function is fitted to data along the rhizome from when xylem maturation is complete; an R 2 for this function is shown. Mean pre‐dawn stem water potentials at the apex and 150 cm from the apex are given. Representative images of transverse sections of a vascular bundle in the stem of E. giganteum at (b) the apex, (c) 120 cm from the apex, and (d) 200 cm from the apex. Sections were stained with aqueous toluidine blue, and images were taken under visible light at ×20 magnification. The arrow in b shows the location of the xylem. Bars, 250 μm. Error bars show ±SE (n = 3).

No change in Dh was observed along the length of the measured terrestrial, prostrate rhizome of P. pseudoaureum (Fig. 4a). Mean rhizome Dh in P. pseudoaureum ranged from 83.07 μm at the rhizome apex to 82.28 μm 40 cm away from the apex (Table 1). Dh in the rhizome of the P. pseudoaureum was the largest of the species examined. By contrast, Dh declined from the base of the stipe towards the apex of the leaf in P. pseudoaureum (Fig. 5a). This decline in Dh across the stipe and into the midrib of the leaf lamina was pronounced, declining from 76.13 μm to 25.07 μm over the span of 55 cm across the frond (Fig. 5a). This tip‐to‐base widening could be explained by a significant two‐parameter power function (R 2 = 0.99, P < 0.001) with an exponent of 0.46 (Fig. 5a; Table 1).

Fig. 4.

Fig. 4

Open in a new tab

No tip‐to‐base conduit widening in the rhizomes of Phlebodium pseudoaureum. (a) Mean hydraulically weighted xylem conduit diameter (Dh) along the terrestrially growing rhizome of P. pseudoaureum; the insert depicts the rhizome of P. pseudoaureum. Representative images of transverse sections of the vascular bundle in the rhizome of P. pseudoaureum at (b) the apex, (c) 20 cm from the apex, and (d) 40 cm from the apex. Sections were stained with aqueous toluidine blue, and images were taken under visible light at ×20 magnification. The arrow in b shows the location of the xylem. Bars, 500 μm. Error bars show ±SE (n = 3).

Fig. 5.

Fig. 5

Open in a new tab

Tip‐to‐base conduit widening across the frond of Phlebodium pseudoaureum. (a) Mean hydraulically weighted xylem conduit diameter (Dh) along the frond of P. pseudoaureum; the insert depicts the frond of P. pseudoaureum. A two‐parameter power function is fitted to the data, and an R 2 for this function is shown. Representative images of transverse sections of a vascular bundle in the rachis or stipe of P. pseudoaureum (b) 5 cm from the apex, (c) 15 cm from the apex, and (d) 60 cm from the apex. Sections were stained with aqueous toluidine blue, and images were taken under visible light at ×10 magnification. The arrow in b shows the location of the xylem. Bars, 500 μm. Error bars show ±SE (n = 3).

Water status

In M. hirsuta we observed that leaf water potential declined with proximity to the apex in rhizomes that grew out of standing water and into air (Table 2; Fig. 2b). Midday leaf water potential was −0.88 MPa at the apex, −0.53 MPa 20 cm from the apex and − 0.42 MPa 40 cm from the apex where the rhizome was in closest proximity to standing water (Table 2; Fig. 1b). Significant differences were also observed in leaf water potential across the vertical stems of E. giganteum (Fig. 3b) with a midday water potential of −1.79 MPa at the apex, but −0.51 MPa in side shoots 120 cm from the apex around the middle of the vertical stem (Table 2). We also observed a significant difference in stem water potential of −0.41 MPa at the apex and −0.12 MPa 120 cm from the apex in E. giganteum (Fig. 3a). No difference in water potential was observed in leaves taken from along the terrestrial, prostrate rhizome of P. pseudoaureum (Fig. 4b) that grew along the soil surface, with mean leaf water potential varying between −0.64 and −0.72 MPa (Table 2).

Table 2.

Mean leaf water potential along the stem or rhizome.

Species Distance from apex (cm) Leaf water potential (MPa) ± SE
Marsilea hirsuta 1 −0.88 ± 0.04a
20 −0.53 ± 0.01b
40 −0.42 ± 0.03c
Equisetum giganteum 1 −1.79 ± 0.17a
120 −0.51 ± 0.04b
Phlebodium pseudoaureum 1 −0.64 ± 0.1a
20 −0.71 ± 0.03a
40 −0.72 ± 0.01a
Open in a new tab

Different letters indicate significant differences in water potential across a rhizome or stem using a post‐hoc pairwise Tukey's test at P < 0.05.

Discussion

Given the primary xylem in ferns, as well as the diversity of growth forms in this group of plants, from arborescent species to those with terrestrial or even aquatic rhizomes, ferns provide an excellent system in which to investigate whether tip‐to‐base conduit widening is adaptively relevant in land plants and to interrogate the mechanism driving this phenomenon. Our observations revealed that tip‐to‐base conduit widening in ferns manifests in rhizomes, stems, or leaves that require the maintenance of hydraulic efficiency along the full pathlength for water flow to the apex, and not in rhizomes or stems that, due to growth habit or environment, do not require long‐distance water transport. Our result suggests that the development of wider conduits away from the apex maintains efficient hydraulic supply in stems and leaves that require it (i.e. vertically growing stems), whereas when there is relaxed pressure on efficient hydraulic supply across the stem (i.e. in aquatic rhizomes or those that root at each node) then alternative scaling functions can manifest without lethal consequence. Interestingly, we found that the exponent of the power function of the relationship between Dh and distance from the apex was similar to a universal value reported widely across vascular plants in M. hirsuta or was higher in the stems of E. giganteum and the fronds of P. pseudoaureum (Table 1). It has been hypothesized that the exponent for this relationship will be higher in leaves so that hydraulic resistance is kept independent of leaf length to ensure that plasticity in leaf size does not influence whole plant hydraulic resistance (Lechthaler et al., 2020), which explains the considerably higher tip‐to‐base widening exponent in the fronds of P. pseudoaureum (Olson et al., 2021). Similarly, the stems of E. giganteum are also the primary photosynthetic organ bearing leaves that are appressed to the stem and numerous side shoots; the increase in size towards the base of the main stem may also serve to counter the increase in the total pathlength for water flow in this species, necessitating a higher exponent.

Most studies show that Dh increases away from the apex to the base of the stem (Zimmermann, 1983; Meinzer et al., 2001; Nijsse et al., 2001; Martínez‐Vilalta et al., 2002; McCulloh & Sperry, 2005; Koçillari et al., 2021), with many concluding that this is an adaptively relevant characteristic of all land plants (Petit, 2024); yet the mechanism driving this anatomical trait remains unknown. Our results suggest that water status might canalize the developmental potential of the xylem such that a universal scaling of conduit diameters towards the apex manifests. In P. pseudoaureum with a rhizome that roots at each node in direct contact with the soil and in the aquatic rhizomes of M. hirsuta, we found that there was no significant variation along the stem in Dh. In these species, leaf water potential remained high in the apex and did not vary across nodes (Table 2). By contrast, Dh declined towards the apex of both the vertical stems of E. giganteum (Fig. 3a–c), the non‐aquatic stems of M. hirsuta (Fig. 2a–c) and across the fronds of P. pseudoaureum (Fig. 5). Only in these tissues, in which hydraulic efficiency needed to be maintained, did we observe tip‐to‐base conduit widening (Table 2; Fig. 3a). Water potential gradients, as well as auxin levels, significantly affect the development of xylem in angiosperms (Aloni & Zimmermann, 1983; Brodribb & Hill, 2000; Johnson et al., 2018), from cell size to wall structure, presumably influencing xylem function and the hydraulic architecture of the individual. In terms of cell size, high turgor pressure appears to be key to driving maximum cell expansion in the meristem (Kazuyuki et al., 1997; Ali et al., 2022).

Our observation that the development of tip‐to‐base conduit widening occurs in aerial stems of M. hirsuta indicates that this developmental phenomenon has not been lost in aquatic species, but will only manifest under conditions that require the maintenance of hydraulic efficiency (Anfodillo & Olson, 2024). Whether these results are generalizable to all aquatic plants remains to be tested, but there are suggestions that an absence of tip‐to‐base conduit widening is common to the stems of numerous aquatic species (Olson pers. comm.). These results also highlight that there is considerable developmental potential in the xylem, but that a universal scaling of tip‐to‐base conduit widening occurs when a buffering of hydraulic resistance along the stem is required. Other studies have shown that there is considerable developmental potential in xylem anatomy regulated by hormones or genes (Aloni & Zimmermann, 1983; Johnson et al., 2018; Rodriguez‐Zaccaro et al., 2021), which might be the primary determinant of this anatomical change, although more work is required to determine the specific mechanism that drives tip‐to‐base conduit widening when organs require it.

The rhizomes of ferns growing on the surface of the soil and rooting at each node or in water, as is the case in P. pseudoaureum and the aquatic rhizomes of M. hirsuta, respectively, are able to maintain a constant water status across the rhizome irrespective of the number of nodes along the rhizome. Fern rhizomes that grow horizontally along the soil surface typically root at each node and distribute nutrients and water evenly across a wide area (Suissa et al., 2023). Lateral distribution of water rather than apical transport means that any tip‐to‐base widening would have no benefit for hydraulic efficiency in these species (Suissa et al., 2023). Suissa et al. (2023) have shown that the phytomers along the rhizomes of terrestrial ferns are hydraulically isolated, suggesting that long‐distance water transport along the rhizome is minimal and that the hydraulic rules governing tip‐to‐base conduit widening in arborescent stems might not apply to these plants. By contrast, if stems grow into drier environments or aboveground, tip‐to‐base conduit widening in these organs will mitigate severe declines in water potential towards the apex if widening did not occur.

Through the use of ferns, we show that tip‐to‐base conduit widening manifests in tissues and organs in which maximizing hydraulic efficiency is paramount; that is, in organs that receive water supply from a single, basal location. Our results suggest that in fern organs in which there is no apical water transport, there is no tip‐to‐base conduit widening. Our results suggest that under conditions in which selection does not favor tip‐to‐base conduit widening for hydraulic efficiency, then a relaxation of developmental potential occurs, whereby conduit diameters tend to approach a maximum rapidly. Our results indicate considerable developmental potential for xylem conduit diameter exists under conditions in which hydraulic efficiency is not required for survival, but that tip‐to‐base conduit widening consistently manifests in organs where there is a need to buffer the resistance of the conductive path as it becomes longer.

Competing interests

None declared.

Author contributions

YK collected and analyzed data and wrote the manuscript; SAMM devised the study and revised the manuscript.

Disclaimer

The New Phytologist Foundation remains neutral with regard to jurisdictional claims in maps and in any institutional affiliations.

Acknowledgements

We thank Mark Olson and Tommaso Anfodillo for valuable comments on the manuscript. Thanks also to Anju Manandhar for assistance with the water potential measurements and data collection as well as all colleagues in the laboratory in fruitful discussion on the topic. We are grateful for the Ukrainian Scholar Program of Purdue University for supporting YK. This work was funded by an NSF grant IOS‐2140119 to SM.

Data availability

All data are included in the manuscript.

References

  1. Ali O, Cheddadi I, Landrein B, Long Y. 2022. Revisiting the relationship between turgor pressure and plant cell growth. New Phytologist 238: 62–69. [DOI] [PubMed] [Google Scholar]
  2. Aloni R, Zimmermann MH. 1983. The control of vessel size and density along the plant axis. Differentiation 24: 203–208. [Google Scholar]
  3. Anfodillo T, Carraro V, Carrer M, Fior C, Rossi S. 2006. Convergent tapering of xylem conduits in different woody species. New Phytologist 169: 279–290. [DOI] [PubMed] [Google Scholar]
  4. Anfodillo T, Deslauriers A, Menardi R, Tedoldi L, Petit G, Rossi S. 2012. Widening of xylem conduits in a conifer tree depends on the longer time of cell expansion downwards along the stem. Journal of Experimental Botany 63: 837–845. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Anfodillo T, Olson ME. 2024. Stretched sapwood, ultra‐widening permeability and ditching da Vinci: revising models of plant form and function. Annals of Botany 134: 19–42. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Baas P, Ewers FW, Davis SD, Wheeler EA. 2004. Evolution of xylem physiology. In: Poole I, Hemsley A, eds. Evolution of plant physiology. London, UK: Elsevier Academic Press, 273–295. [Google Scholar]
  7. Becker P, Gribben RJ, Lim CM. 2000. Tapered conduits can buffer hydraulic conductance from path‐length effects. Tree Physiology 20: 965–967. [DOI] [PubMed] [Google Scholar]
  8. Bierhorst DW. 1960. The xylem as evidence for the filicinean ancestry of the Angiosperms. American Journal of Botany 47: 401–409. [Google Scholar]
  9. Bok ECPM, Brodribb TJ, Jordan GJ, Carriquí M. 2022. Convergent tip‐to‐base widening of water‐conducting conduits in the tallest bryophytes. American Journal of Botany 109: 322–332. [DOI] [PubMed] [Google Scholar]
  10. Brodribb T, Mencuccini M. 2017. Xylem. In: Thomas B, Murray BG, Murphy DJ, eds. Encyclopedia of applied plant sciences, vol. 1. London, UK: Elsevier Academic Press, 141–148. [Google Scholar]
  11. Brodribb TJ, Hill RS. 2000. Increases in water potential gradient reduce xylem conductivity in whole plants. Evidence from a low‐pressure conductivity method. Plant Physiology 123: 1021–1027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Cabon A, Fernández‐de‐Uña L, Gea‐Izquierdo G, Meinzer FC, Woodruff DR, Martínez‐Vilalta J, De Cáceres M. 2020. Water potential control of turgor‐driven tracheid enlargement in Scots pine at its xeric distribution edge. New Phytologist 225: 209–221. [DOI] [PubMed] [Google Scholar]
  13. Carlquist S, Schneider E. 2001. Vessels in ferns: structural, ecological, and evolutionary significance. American Journal of Botany 88: 1–13. [PubMed] [Google Scholar]
  14. Chambers‐Ostler A, Gloor E, Galbraith D, Groenendijk P, Brienen R. 2023. Vessel tapering is conserved along a precipitation gradient in tropical trees of the genus Cedrela. Trees 37: 269–284. [Google Scholar]
  15. Chave J, Coomes D, Jansen S, Lewis SL, Swenson NG, Zanne AE. 2009. Towards a worldwide wood economics spectrum. Ecology Letters 12: 351–366. [DOI] [PubMed] [Google Scholar]
  16. Couvreur V, Ledder G, Manzoni S, Way DA, Muller EB, Russo SE. 2018. Water transport through tall trees: a vertically explicit, analytical model of xylem hydraulic conductance in stems. Plant, Cell & Environment 41: 1–19. [DOI] [PubMed] [Google Scholar]
  17. Drobnitch ST, Jensen KH, Prentice P, Pittermann J. 2015. Convergent evolution of vascular optimization in kelp (Laminariales). Proceedings of the Royal Society B: Biological Sciences 282: 20151667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hacke UG, Sperry JS, Wheeler JK, Castro L. 2006. Scaling of angiosperm xylem structure with safety and efficiency. Tree Physiology 26: 689–701. [DOI] [PubMed] [Google Scholar]
  19. Husby CE. 2009. Ecophysiology and biomechanics of Equisetum giganteum in South America. FIU Electronic Theses and Dissertations. Paper 200. [WWW document] URL https://digitalcommons.fiu.edu/etd/200 [accessed 20 May 2025].
  20. James SA, Meinzer FC, Goldstein G, Woodruff D, Jones T, Restom T, Mejia M, Clearwater M, Campanello P. 2003. Axial and radial water transport and internal water storage in tropical forest canopy trees. Oecologia 134: 37–45. [DOI] [PubMed] [Google Scholar]
  21. Johnson D, Eckart P, Alsamadisi N, Noble H, Martin C, Spicer R. 2018. Polar auxin transport is implicated in vessel differentiation and spatial patterning during secondary growth in Populus . American Journal of Botany 105: 186–196. [DOI] [PubMed] [Google Scholar]
  22. Kazuyuki H, Masao M, Takeshi I. 1997. Effects of higher turgor pressure on plant cell expansion. Plant Physiology 115: 627–634. [Google Scholar]
  23. Koçillari L, Olson ME, Suweis S, Rocha RP, Lovison A, Cardin F, Dawson TE, Echeverría A, Fajardo A, Lechthaler S et al. 2021. The widened pipe model of plant hydraulic evolution. Proceedings of the National Academy of Sciences, USA 118: e2100314118. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kolb KJ, Sperry JS. 1999. Differences in drought adaptation between subspecies of sagebrush (Artemisia tridentata). Ecology 80: 2373–2384. [Google Scholar]
  25. Lechthaler S, Kiorapostolou N, Pitacco A, Anfodillo T, Petit G. 2020. The total path length hydraulic resistance according to known anatomical patterns: what is the shape of the root‐to‐leaf tension gradient along the plant longitudinal axis? Journal of Theoretical Biology 502: e110369. [DOI] [PubMed] [Google Scholar]
  26. Lens F, Tixier A, Cochard H, Sperry JS, Jansen S, Herbette S. 2013. Embolism resistance as a key mechanism to understand adaptive plant strategies. Current Opinion in Plant Biology 16: 287–292. [DOI] [PubMed] [Google Scholar]
  27. Mahley JN, Watkins JE, Holbrook NM, Zwieniecki MA. 2018. Geometry, allometry and biomechanics of fern leaf petioles: Their significance for the evolution of functional and ecological diversity within the Pteridaceae. Frontiers in Plant Science 9: 197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Martínez‐Vilalta J, Prat E, Oliveras I, Piñol J. 2002. Xylem hydraulic properties of roots and stems of nine Mediterranean woody species. Oecologia 133: 19–29. [DOI] [PubMed] [Google Scholar]
  29. McCulloh KA, Sperry JS. 2005. Patterns in hydraulic architecture and their implications for transport efficiency. Tree Physiology 25: 257–267. [DOI] [PubMed] [Google Scholar]
  30. Meinzer FC, Clearwater MJ, Goldstein G. 2001. Water transport in trees: current perspectives, new insights and some controversies. Environmental and Experimental Botany 45: 239–262. [DOI] [PubMed] [Google Scholar]
  31. Meinzer FC, McCulloh KA, Lachenbruch B, Woodruff DR, Johnson DM. 2010. The blind men and the elephant: the impact of context and scale in evaluating conflicts between plant hydraulic safety and efficiency. Oecologia 164: 287–296. [DOI] [PubMed] [Google Scholar]
  32. Nijsse J, van der Heijden GW, van Ieperen W, Keijzer CJ, van Meeteren U. 2001. Xylem hydraulic conductivity related to conduit dimensions along chrysanthemum stems. Journal of Experimental Botany 52: 319–327. [PubMed] [Google Scholar]
  33. Olson ME, Anfodillo T, Gleason SM, McCulloh KA. 2021. Tip‐to‐base xylem conduit widening as an adaptation: causes, consequences, and empirical priorities. New Phytologist 229: 1877–1893. [DOI] [PubMed] [Google Scholar]
  34. Olson ME, Anfodillo T, Rosell JA, Petit G, Crivellaro A, Isnard S, León‐Gómez C, Alvarado‐Cárdenas LO, 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. [DOI] [PubMed] [Google Scholar]
  35. Olson ME, Arroyo‐Santos A. 2015. How to study adaptation (and why to do it that way). Quarterly Review of Biology 90: 167–191. [DOI] [PubMed] [Google Scholar]
  36. Olson ME, Soriano D, Rosell JA, Anfodillo T, Donoghue MJ, Edwards EJ, León‐Gómez C, Dawson T, Camarero Martínez JJ, Castorena M et al. 2018. Plant height and hydraulic vulnerability to drought and cold. Proceedings of the National Academy of Sciences, USA 115: 7551–7556. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Petit G. 2024. An appreciation of apex‐to‐base variation in xylem traits will lead to more precise understanding of xylem phenotypic plasticity. New Phytologist 244: 1175–1180. [DOI] [PubMed] [Google Scholar]
  38. Petit G, Anfodillo T. 2009. Plant physiology in theory and practice: an analysis of the WBE model for vascular plants. Journal of Theoretical Biology 259: 1–4. [DOI] [PubMed] [Google Scholar]
  39. Pittermann J, Brodersen C, Watkins JE. 2013. The physiological resilience of fern sporophytes and gametophytes: advances in water relations offer new insights into an old lineage. Frontiers in Plant Science 4: 1–10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Ray PM, Green PB. 1972. Role of turgor in the growth of plant cells. Nature: New Biology 235: 24–26.4502406 [Google Scholar]
  41. Rodriguez‐Dominguez CM, Forner A, Martorell S, Choat B, Lopez R, Peters JMR, Pfautsch S, Mayr S, Carins‐Murphy MR. 2022. Leaf water potential measurements using the pressure chamber: synthetic testing of assumptions towards best practices for precision and accuracy. Tree Physiology 42: 1133–1147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Rodriguez‐Zaccaro FD, Henry IM, Groover A. 2021. Genetic regulationof vessel morphology in Populus . Frontiers in Plant Science 12: 705596. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Rosell JA, Olson ME. 2014. Do lianas really have wide vessels? Vessel diameter–stem length scaling in non‐self‐supporting plants. Perspectives in Plant Ecology, Evolution and Systematics 16: 288–295. [Google Scholar]
  44. Rosell JA, Olson ME, Anfodillo T. 2017. Scaling of xylem vessel diameter with plant size: causes, predictions, and outstanding questions. Current Forestry Reports 3: 46–59. [Google Scholar]
  45. Sack L, Holbrook NM. 2006. Leaf hydraulics. Annual Review of Plant Biology 57: 361–381. [DOI] [PubMed] [Google Scholar]
  46. Sanio K. 1872. Ueber die Grösse der Holzzellen bei gemeiner Kiefer (Pinus sylvestris). Jahrbucher fur Wissenschaftliche Botanik 8: 401–420. [Google Scholar]
  47. Savage VM, Bentley LP, Enquist BJ, Sperry JS, Smith DD, Reich PB, von Allmen EI. 2010. Hydraulic trade‐offs and space filling enable better predictions of vascular structure and function in plants. Proceedings of the National Academy of Sciences, USA 107: 22722–22727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Schindelin J, Arganda‐Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B et al. 2012. Fiji: an open‐source platform for biological‐image analysis. Nature Methods 9: 676–682. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Schneider EL, Carlquist S. 2000b. SEM studies on vessels in ferns. 19. Marsilea. American Fern Journal 90: 32–41. [PubMed] [Google Scholar]
  50. Schneider H, Pryer KM. 2002. Structure and function of spores in the aquatic heterosporous fern family Marsileaceae. International Journal of Plant Sciences 163: 485–505. [Google Scholar]
  51. Smith AR, Pryer KM, Schuettpelz E, Korall P, Schneider H, Wolf P. 2008. Fern Classification. In: Ranker TA, Haufler CH, eds. Biology and evolution of ferns and lycophytes. Cambridge, UK: Cambridge University Press, 417–467. [Google Scholar]
  52. Sperry JS, Hacke UG, Oren R, Comstock JP. 2002. Water deficits and hydraulic limits to leaf water supply. Plant, Cell & Environment 25: 251–263. [DOI] [PubMed] [Google Scholar]
  53. Sperry JS, Nichols KL, Sullivan JE, Eastlack M. 1994. Xylem embolism in ring porous, diffuse porous and coniferous trees of northern Utah and interior Alaska. Ecology 75: 1736–1752. [Google Scholar]
  54. Suissa JS, Agbleke AA, Friedman WE. 2023. A bump in the node: the hydraulic implications of rhizomatous growth. American Journal of Botany 110: 16105. [DOI] [PubMed] [Google Scholar]
  55. Suissa JS, Friedman WE. 2021. From cells to stems: the effects of primary vascular construction on drought‐induced embolism in fern rhizomes. New Phytologist 232: 2238–2253. [DOI] [PubMed] [Google Scholar]
  56. Tejero‐Díez JD, Mickel JT, Smith AR. 2009. A hybrid Phlebodium (Polypodiaceae, Polypodiophyta) and its influence on the circumscription of the genus. American Fern Journal 99: 109–116. [Google Scholar]
  57. Tyree MT, Zimmermann MH. 2002. Hydraulic architecture of whole plants and plant performance. In: Xylem structure and the ascent of sap. Berlin, Germany: Springer, 175–214. [Google Scholar]
  58. Vasco A, Moran RC, Ambrose AAR. 2013. The evolution, morphology, and development of fern leaves. Frontiers in Plant Science 4: 345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. West GB, Brown JH, Enquist BJ. 1997. A general model for the origin of allometric scaling laws in biology. Science 276: 122–126. [DOI] [PubMed] [Google Scholar]
  60. West GB, Brown JH, Enquist BJ. 1999. A general model for the structure and allometry of plant vascular systems. Nature 400: 664–667. [Google Scholar]
  61. Westbrook AS, McAdam SAM. 2021. Stomatal density and mechanics are critical for high productivity: insights from amphibious ferns. New Phytologist 229: 877–889. [DOI] [PubMed] [Google Scholar]
  62. White RA. 1963. Tracheary elements of the ferns. II.:Morphology oftracheary elements; conclusions. American Journal of Botany 50: 514–522. [Google Scholar]
  63. Zimmermann MH. 1983. Xylem structure and the ascent of sap. Berlin, Germany: Springer‐Verlag, 149. [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

All data are included in the manuscript.

Articles from The New Phytologist are provided here courtesy of Wiley

RESOURCES