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Advanced vascular function discovered in a widespread moss

Nature Plants volume 6, pages 273–279 (2020)Cite this article

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Abstract

The evolution of terrestrial plants capable of growing upwards into the dry atmosphere profoundly transformed the Earth. A transition from small, ‘non-vascular’ bryophytes to arborescent vascular plants during the Devonian period is partially attributed to the evolutionary innovation of an internal vascular system capable of functioning under the substantial water tension associated with vascular water transport. Here, we show that vascular function in one of the most widespread living bryophytes (Polytrichum commune) exhibits strong functional parallels with the vascular systems of higher plants. These parallels include vascular conduits in Polytrichum that resist buckling while transporting water under tension, and leaves capable of regulating transpiration, permitting photosynthetic gas exchange without cavitation inside the vascular system. The advanced vascular function discovered in this tallest bryophyte family contrasts with the highly inefficient water use found in their leaves, emphasizing the importance of stomatal evolution enabling photosynthesis far above the soil surface.

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Fig. 1: P. commune vascular tissue is capable of sustaining large hydraulic tension without collapsing.
Fig. 2: The water transport system in P. commune shows a pattern of vulnerability to cavitation-induced failure similar to that seen in vascular plants.
Fig. 3: Similar to vascular plants, the leaves of P. commune regulate water loss during water stress to delay the onset of damaging cavitation in the water transport system.
Fig. 4: Compared to vascular plants, photosynthesis in P. commune is highly sensitive to humidity as a result of its intrinsically inefficient exchange of water vapour for CO2.

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All processed data are contained in the manuscript or Extended Data. Raw images and image sequences can be supplied upon request from the corresponding author.

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Acknowledgements

We thank A. Graham at the Harvard Center for Nanoscale Studies for his expert technical assistance with Cryo-SEM. We acknowledge the SOLEIL synchrotron, Saclay, France for provision of synchrotron radiation beamtime at the PSICHE beamline, and thank A. King for assistance. This research was funded by an Australian Research Council Discovery Grant (no. DP 170100761 awarded to T.J.B.). M.C. received a travel grant from La Caixa Banking Foundation and from the Conselleria d’Educació i Universitats (Govern de les Illes Balears) and European Social Fund (predoctoral fellowship no. FPI/1700/2014). N.M.H. was supported by a Visiting Scholar award from the University of Tasmania, and NSF grants nos. IOS-1659918 and DMR-1420570 studies. This work was supported by the programme Investments for the Future (nos. ANR-10-EQPX-16, XYLOFOREST and Labex COTE) from the French National Agency for Research.

Author information

Authors and Affiliations

  1. School of Natural Sciences, University of Tasmania, Hobart, Tasmania, Australia

    T. J. Brodribb & M. Carriquí

  2. Research Group on Plant Biology under Mediterranean Conditions, Departament de Biologia, Universitat de les Illes Balears – Instituto de Investigaciones Agroambientales y de la Economía del Agua, Palma, Spain

    M. Carriquí

  3. Université Bordeaux, BIOGECO, INRAE, Pessac, France

    S. Delzon

  4. Purdue Center for Plant Biology, Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN, USA

    S. A. M. McAdam

  5. Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA

    N. M. Holbrook

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Contributions

T.J.B., M.C. and N.M.H. designed the study. T.J.B., N.M.H., M.C. and S.D. carried out the experiments. T.J.B. wrote the manuscript with input from N.M.H., M.C., S.D. and S.A.M.M. S.A.M.M. provided additional data.

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Correspondence to T. J. Brodribb or N. M. Holbrook.

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Peer review information Nature Plants thanks Jeffrey Duckett, Karen Renzaglia and the other, anonymous, reviewer for their contribution to the peer review of this work.

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Extended data

Extended Data Fig 1 Coordinated hydraulic conductance and assimilation.

The mean shoot hydraulic conductance and mean photosynthetic capacity of Polytrichum commune ( + /- SD, n = 7 individuals) measured here (triangle) falls close to the relationship found in leaves from the major groups of vascular plants; lycophytes and ferns (green), seed plants (blue) (published data from (27)).

Extended Data Fig 2 Above and below ground hydraulic resistance.

The distribution of hydraulic resistances as a percentage of total resistance (grey bars + SD, n = 7) between belowground (rhizoid) and aboveground (shoot) tissues in Polytrichum commune plants. Absolute values of hydraulic conductance (means shown as green bars, + SD, n = 7) show considerable variation, but the split between tissues is similar.

Extended Data Fig 3 Shoot hydraulic vulnerability.

The hydraulic conductance of Polytrichum commune shoots (Kshoot) was observed to decline sharply upon exposure to water stress. Each point represents a separate plant (n = 18 individuals) subjected to different degrees of dehydration stress. A rapid decline of Kshoot between -1 and −2MPa matched the observed pattern of cavitation using visual methods (Fig. 2). The form of the sigmoidal function fitted here was used in the hydraulic model used in Fig. 3.

Extended Data Fig 4 Refilling kinetics in Polytrichum.

Hydroids of the central strand of a single Polytrichum commune caulidium are shown to refill after a droughted plant that had fully cavitated was rehydrated after several hours ( > 12) after the last cavitation event was observed. Data from a single individual stem from an intact plant shows that 90 min after rewatering from both phyllidia and rhizome the hydroids begin to effectively refill with water, compressing the air into nanobubbles (which should dissolve over time) at around 125 min after rewatering of the plant. Average relative hydroid refilling state (proportion of water present in hydroids) over time is shown as black dots, while individual hydroid refilling states for each hydroid are shown as grey dots.

Extended Data Fig 5 Dynamic response to humidity in Polytrichum gas exchange.

Dynamic changes in photosynthetic assimilation rate and leaf diffusive conductance to water vapor during a transition from a vapor pressure deficit of 1.5 kPa (approximately 50% RH) to 3 kPa (approximately 5% RH). The pink box shows measurements made at 3 kPa, after which vapor pressure deficit was decreased to 1.0 kPa and recovery recorded. A rapid reduction in diffusive conductance and photosynthesis is evident upon exposure to drier air, while a complete recovery occurs upon return to more humid conditions. Changes in photosynthetic assimilation (A) measured by gas analysis correspond with changes in photosynthetic electron transport rate (ETR) measured by chlorophyll fluorescence (graph insert).

Extended Data Fig 6 Leaf movement in response to dehydration in Polytrichum.

As shoots of Polytrichum commune desiccate, leaves move from a position that is perpendicular to the stem (image top right) to being arranged parallel to the stem (image lower right). The relationship between leaf angle and ψshoot for five individuals subjected to slow desiccation (each color represents a different replicate plant) shows a rapid decline in leaf angle as ψshoot fell from 0 to −1.5 MPa. This pattern of decline matched closely the pattern of declining diffusive conductance seen in Fig. 3.

Extended Data Fig 7 Humidity sensitivity of assimilation.

Sensitivity of absolute assimilation rate to VPD in P. commune (open circles) and vascular plants (black points).

Extended Data Fig 8 Table of humidity sensitivity in diverse species.

Steady state leaf gas exchange across variable vapor pressure differences for vascular plant species taken from the literature.

Extended Data Fig 9 Table of maximum photosynthetic gas exchange in diverse species.

Maximum rates of gas exchange collected under standard conditions for species of lycophyte and ferns taken from the literature or measured in this study.

Supplementary information

Reporting Summary

Supplementary Video 1

Rehydration and refilling of hydroids as described in Extended Data Fig. 4. Similar results were found for all samples (n = 3).

Source data

Source Data Fig. 1

Anatomy data.

Source Data Fig. 2

Optical vulnerability data.

Source Data Fig. 3

Gas exchange in Polytrichum.

Source Data Fig. 4

Gas exchange in all species.

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Brodribb, T.J., Carriquí, M., Delzon, S. et al. Advanced vascular function discovered in a widespread moss. Nat. Plants 6, 273–279 (2020). https://doi.org/10.1038/s41477-020-0602-x

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