Advanced vascular function discovered in a widespread moss.
Journal
Nature plants
ISSN: 2055-0278
Titre abrégé: Nat Plants
Pays: England
ID NLM: 101651677
Informations de publication
Date de publication:
03 2020
03 2020
Historique:
received:
14
08
2019
accepted:
22
01
2020
entrez:
15
3
2020
pubmed:
15
3
2020
medline:
15
12
2020
Statut:
ppublish
Résumé
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.
Identifiants
pubmed: 32170283
doi: 10.1038/s41477-020-0602-x
pii: 10.1038/s41477-020-0602-x
doi:
Substances chimiques
Water
059QF0KO0R
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
273-279Commentaires et corrections
Type : CommentIn
Références
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).
pubmed: 17443185
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).
pubmed: 28985561
Xu, B. et al. Contribution of NAC transcription factors to plant adaptation to land. Science 343, 1505–1508 (2014).
pubmed: 24652936
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).
pubmed: 30136925
pmcid: 6141232
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).
pubmed: 28013230
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).
pubmed: 20642725
Espiñeira, J. et al. Distribution of lignin monomers and the evolution of lignification among lower plants. Plant Biol. 13, 59–68 (2011).
pubmed: 21143726
Martin StPaul, N., Delzon, S. & Cochard, H. Plant resistance to drought depends on timely stomatal closure. Ecol. Lett. 20, 1437–1447 (2017).
pubmed: 28922708
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).
pubmed: 17556506
pmcid: 1949879
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).
pubmed: 12651550
Sperry, J. S. & Tyree, M. T. Mechanism of water stress-induced xylem embolism. Plant Physiol. 88, 581–587 (1988).
pubmed: 16666352
pmcid: 1055628
Choat, B. et al. Global convergence in the vulnerability of forests to drought. Nature 491, 752 (2012).
pubmed: 23172141
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).
pubmed: 20525002
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).
pubmed: 29748980
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).
pubmed: 17938107
Rolland, V. et al. Easy come, easy go: capillary forces enable rapid refilling of embolized primary xylem vessels. Plant Physiol. 168, 1636–1647 (2015).
pubmed: 26091819
pmcid: 4528742
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).
pubmed: 11788773
pmcid: 148995
Brodribb, T. J. & McAdam, S. A. Evolution of the stomatal regulation of plant water content. Plant Physiol. 174, 639–649 (2017).
pubmed: 28404725
pmcid: 5462025
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).
pubmed: 30623444
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).
pubmed: 19011001
pmcid: 2613726
Brodribb, T. J., Carriqui, M., Delzon, S. & Lucani, C. Optical measurement of stem xylem vulnerability. Plant Physiol. 174, 2054–2061 (2017).
pubmed: 28684434
pmcid: 5543975
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).
pubmed: 12651346
King, A. et al. Tomography and imaging at the PSICHE beam line of the SOLEIL synchrotron. Rev. Sci. Instrum. 87, 093704 (2016).
pubmed: 27782575
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).
pubmed: 12000561
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).
pubmed: 23421706
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).
pubmed: 27208264
pmcid: 4936570
Brodribb, T. J. & McAdam, S. A. M. Passive origins of stomatal control in vascular plants. Science 331, 582–585 (2011).
pubmed: 21163966
McAdam, S. A. M. & Brodribb, T. J. Separating active and passive influences on stomatal control of transpiration. Plant Physiol. 164, 1578–1586 (2014).
pubmed: 24488969
pmcid: 3982724
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).
pubmed: 25637454
pmcid: 4348763
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).
pubmed: 30566632
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).
pubmed: 22682564
Doi, M., Kitagawa, Y. & Shimazaki, K.-i Stomatal blue light response is present in early vascular plants. Plant Physiol. 169, 1205–1213 (2015).
pubmed: 26307440
pmcid: 4587438
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).
pubmed: 26602987
pmcid: 4689120
Tosens, T. et al. The photosynthetic capacity in 35 ferns and fern allies: mesophyll CO
pubmed: 26508678