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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Kenrick, P. & Crane, P. R. The origin and early evolution of plants on land. Nature 389, 33–39 (1997).
Edwards, D., Davies, K. L. & Axe, L. A vascular conducting strand in the early land plant Cooksonia. Nature 357, 683–685 (1992).
Lang, W. H. IV—On the plant-remains from the Downtonian of England and Wales. Philos. Trans. R. Soc. Lond. B 227, 245–291 (1937).
Renzaglia, K., McFarland, K. & Smith, D. Anatomy and ultrastructure of the sporophyte of Takakia ceratophylla (Bryophyta). Am. J. Bot. 84, 1337–1350 (1997).
Stein, W. E., Mannolini, F., Hernick, L. V., Landing, E. & Berry, C. M. Giant cladoxylopsid trees resolve the enigma of the Earth’s earliest forest stumps at Gilboa. Nature 446, 904–907 (2007).
Harrison, C. J. & Morris, J. L. The origin and early evolution of vascular plant shoots and leaves. Phil. Trans. R. Soc. Lond. B 373, 20160496 (2017).
Carlquist, S. J. Ecological Strategies of Xylem Evolution (Univ. of California Press, 1975).
Raven, J. A. Evolution of vascular land plants in relation to supracellular transport processes. Adv. Bot. Res. 5, 153–219 (1977).
Duckett, J. G. & Pressel, S. The evolution of the stomatal apparatus: intercellular spaces and sporophyte water relations in bryophytes—two ignored dimensions. Phil. Trans. R. Soc. B 373, 20160498 (2017).
Bowman, J. L. et al. Insights into land plant evolution garnered from the Marchantia polymorpha genome. Cell 171, 287–304 (2017).
Xu, B. et al. Contribution of NAC transcription factors to plant adaptation to land. Science 343, 1505–1508 (2014).
Honkanen, S., Thamm, A., Arteaga-Vazquez, M. A. & Dolan, L. Negative regulation of conserved RSL class I bHLH transcription factors evolved independently among land plants. eLife 7, e38529 (2018).
Ohtani, M., Akiyoshi, N., Takenaka, Y., Sano, R. & Demura, T. Evolution of plant conducting cells: perspectives from key regulators of vascular cell differentiation. J. Exp. Bot. 68, 17–26 (2017).
Hébant, C. The Conducting Tissues of Bryophytes (J. Cramer, 1977).
Edwards, D., Axe, L. & Duckett, J. Diversity in conducting cells in early land plants and comparisons with extant bryophytes. Bot. J. Linn. Soc. 141, 297–347 (2003).
Haberlandt, G. Beiträge zur Anatomie und Physiologie der Laubmoose. Jahrb. Wiss. Bot. 17, 359–498 (1886).
Tansley, A. G. & Chick, E. Notes on the conducting tissue-system in Bryophyta. Ann. Bot. 15, 1–38 (1901).
Atala, C. Water transport and gas exchange in the non-vascular plant Dendroligotrichum dendroides (Brid. ex Hedw.) Broth. (Polytrichaceae, Bryophyta). Gayana Bot. 68, 89–92 (2011).
Blaikley, N. M. Absorption and conduction of water and transpiration in Polytrichum commune. Ann. Bot. 46, 289–300 (1932).
Ligrone, R., Duckett, J. & Renzaglia, K. Conducting tissues and phyletic relationships of bryophytes. Phil. Trans. R. Soc. Lond. B 355, 795–813 (2000).
Vanderpoorten, A. & Goffinet, B. Introduction to Bryophytes (Cambridge Univ. Press, 2009).
Tyree, M. T. & Zimmermann, M. H. Xylem Structure and the Ascent of Sap (Springer Science & Business Media, 2013).
Weng, J. K. & Chapple, C. The origin and evolution of lignin biosynthesis. New Phytol. 187, 273–285 (2010).
Espiñeira, J. et al. Distribution of lignin monomers and the evolution of lignification among lower plants. Plant Biol. 13, 59–68 (2011).
Martin StPaul, N., Delzon, S. & Cochard, H. Plant resistance to drought depends on timely stomatal closure. Ecol. Lett. 20, 1437–1447 (2017).
Ligrone, R., Carafa, A., Duckett, J., Renzaglia, K. & Ruel, K. Immunocytochemical detection of lignin-related epitopes in cell walls in bryophytes and the charalean alga Nitella. Plant Syst. Evol. 270, 257–272 (2008).
Brodribb, T. J., Feild, T. S. & Jordan, G. J. Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiol. 144, 1890–1898 (2007).
Becker, P., Tyree, M. T. & Tsuda, M. Hydraulic conductances of angiosperms versus conifers: similar transport sufficiency at the whole-plant level. Tree Physiol. 19, 445–452 (1999).
Sperry, J. S. & Tyree, M. T. Mechanism of water stress-induced xylem embolism. Plant Physiol. 88, 581–587 (1988).
Choat, B. et al. Global convergence in the vulnerability of forests to drought. Nature 491, 752 (2012).
Lenne, T., Bryant, G., Hocart, C. H., Huang, C. X. & Ball, M. C. Freeze avoidance: a dehydrating moss gathers no ice. Plant Cell Environ. 33, 1731–1741 (2010).
Cardoso, A. A., Brodribb, T. J., Lucani, C. J., DaMatta, F. M. & McAdam, S. A. Coordinated plasticity maintains hydraulic safety in sunflower leaves. Plant Cell Environ. 41, 2567–2576 (2018).
Cochard, H., Casella, E. & Mencuccini, M. Xylem vulnerability to cavitation varies among poplar and willow clones and correlates with yield. Tree Physiol. 27, 1761–1767 (2007).
Rolland, V. et al. Easy come, easy go: capillary forces enable rapid refilling of embolized primary xylem vessels. Plant Physiol. 168, 1636–1647 (2015).
Cochard, H., Coll, L., Le Roux, X. & Améglio, T. Unraveling the effects of plant hydraulics on stomatal closure during water stress in walnut. Plant Physiol. 128, 282–290 (2002).
Brodribb, T. J. & McAdam, S. A. Evolution of the stomatal regulation of plant water content. Plant Physiol. 174, 639–649 (2017).
Bayfield, N. G. Notes on water relations of Polytrichum commune Hedw. J. Bryol. 7, 607–617 (1973).
Clayton-Greene, K., Collins, N., Green, T. & Proctor, M. Surface wax, structure and function in leaves of Polytrichaceae. J. Bryol. 13, 549–562 (1985).
Carriquí, M. et al. Anatomical constraints to non-stomatal diffusion conductance and photosynthesis in lycophytes and bryophytes. New Phytol. https://doi.org/10.1111/nph.15675 (2019).
Pressel, S. & Duckett, J. G. Do motile spermatozoids limit the effectiveness of sexual reproduction in bryophytes? Not in the liverwort Marchantia polymorpha. J. Syst. Evol. 57, 371–381 (2019).
Essig, F. B. Plant Life: A Brief History (Oxford Univ. Press, 2015).
Brodribb, T. J. & Cochard, H. Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiol. 149, 575–584 (2009).
Brodribb, T. J., Carriqui, M., Delzon, S. & Lucani, C. Optical measurement of stem xylem vulnerability. Plant Physiol. 174, 2054–2061 (2017).
Sarafis, V. A biological account of Polytrichum commune. N. Z. J. Bot. 9, 711–724 (1971).
Pammenter, Nv & Van der Willigen, C. A mathematical and statistical analysis of the curves illustrating vulnerability of xylem to cavitation. Tree Physiol. 18, 589–593 (1998).
King, A. et al. Tomography and imaging at the PSICHE beam line of the SOLEIL synchrotron. Rev. Sci. Instrum. 87, 093704 (2016).
Paganin, D., Mayo, S., Gureyev, T. E., Miller, P. R. & Wilkins, S. W. Simultaneous phase and amplitude extraction from a single defocused image of a homogeneous object. J. Microsc. 206, 33–40 (2002).
Mirone, A., Brun, E., Gouillart, E., Tafforeau, P. & Kieffer, J. The PyHST2 hybrid distributed code for high speed tomographic reconstruction with iterative reconstruction and a priori knowledge capabilities. Nucl. Instrum. Methods Phys. Res. B 324, 41–48 (2014).
Van den Honert, T. Water transport in plants as a catenary process. Discuss. Faraday Soc. 3, 146–153 (1948).
McAdam, S. A. M. & Brodribb, T. J. Ancestral stomatal control results in a canalization of fern and lycophyte adaptation to drought. New Phytol. 198, 429–441 (2013).
McAdam, S. A. M. & Brodribb, T. J. Linking turgor with ABA biosynthesis: implications for stomatal responses to vapour pressure deficit across land plants. Plant Physiol. 171, 2008–2016 (2016).
Brodribb, T. J. & McAdam, S. A. M. Passive origins of stomatal control in vascular plants. Science 331, 582–585 (2011).
McAdam, S. A. M. & Brodribb, T. J. Separating active and passive influences on stomatal control of transpiration. Plant Physiol. 164, 1578–1586 (2014).
McAdam, S. A. M. & Brodribb, T. J. The evolution of mechanisms driving the stomatal response to vapour pressure deficit. Plant Physiol. 167, 833–843 (2015).
Campany, C. E., Martin, L. & Watkins, J. J. E. Convergence of ecophysiological traits drives floristic composition of early lineage vascular plants in a tropical forest floor. Ann. Bot. 123, 793–803 (2019).
Soni, D. K. et al. Photosynthetic characteristics and the response of stomata to environmental determinants and ABA in Selaginella bryopteris, a resurrection spike moss species. Plant Sci. 191–192, 43–52 (2012).
Doi, M., Kitagawa, Y. & Shimazaki, K.-i Stomatal blue light response is present in early vascular plants. Plant Physiol. 169, 1205–1213 (2015).
Zier, J., Belanger, B., Trahan, G. & Watkins, J. E. Ecophysiology of four co-occurring lycophyte species: an investigation of functional convergence. AoB Plants 7, plv137 (2015).
Tosens, T. et al. The photosynthetic capacity in 35 ferns and fern allies: mesophyll CO2 diffusion as a key trait. New Phytol. 209, 1576–1590 (2016).
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.
The authors declare they have no competing interests.
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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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)).
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.
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.
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.
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).
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.
Sensitivity of absolute assimilation rate to VPD in P. commune (open circles) and vascular plants (black points).
Steady state leaf gas exchange across variable vapor pressure differences for vascular plant species taken from the literature.
Maximum rates of gas exchange collected under standard conditions for species of lycophyte and ferns taken from the literature or measured in this study.
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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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