Drought-induced lacuna formation in the stem causes hydraulic conductance to decline before xylem embolism in Selaginella.

ABA embolism evolution hydraulic conductance lycophyte stomatal conductance stomatal evolution

Journal

The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884

Informations de publication

Date de publication:
09 2020
Historique:
received: 18 03 2020
accepted: 22 04 2020
pubmed: 10 5 2020
medline: 15 5 2021
entrez: 10 5 2020
Statut: ppublish

Résumé

Lycophytes are the earliest diverging extant lineage of vascular plants, sister to all other vascular plants. Given that most species are adapted to ever-wet environments, it has been hypothesized that lycophytes, and by extension the common ancestor of all vascular plants, have few adaptations to drought. We investigated the responses to drought of key fitness-related traits such as stomatal regulation, shoot hydraulic conductance (K

Identifiants

pubmed: 32386326
doi: 10.1111/nph.16649
doi:

Substances chimiques

Water 059QF0KO0R

Types de publication

Journal Article Research Support, N.I.H., Extramural 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

1804-1817

Informations de copyright

© 2020 The Authors. New Phytologist © 2020 New Phytologist Trust.

Références

Ambrose BA. 2013. The morphology and development of lycophytes. Annual Plant Reviews 45: 91-114.
Barclay BD. 1931. Origin and development of tissues in stem of Selaginella wildenovii. Botanical Gazette 91: 452-461.
Biggs AR, Miles NW. 1984. Suberin deposition as a measure of wound response in peach bark. HortScience 20: 902-905.
Biggs AR, Miles NW. 1988. Association of suberin formation in uninoculated wounds with susceptibility to Leucostoma cincta and L. persoonii in various peach cultivars. Phytopathology 78: 1070-1074.
Brodersen C, Jansen S, Choat B, Rico C, Pittermann J. 2014. Cavitation resistance in seedless vascular plants: the structure and function of interconduit pit membranes. Plant Physiology 165: 895-904.
Brodersen CR, Rico C, Guenni O, Pittermann J. 2016. Embolism spread in the primary xylem of Polystichum munitum: implications for water transport during seasonal drought. Plant Cell & Environment 39: 338-346.
Brodribb TJ, Bienaimé D, Marmottant P. 2016a. Revealing catastrophic failure of leaf networks under stress. Proceedings of the National Academy of Sciences, USA 113: 4865-4869.
Brodribb TJ, Cochard H. 2009. Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiology 149: 575-584.
Brodribb TJ, Holbrook NM. 2003. Stomatal closure during leaf dehydration, correlation with other leaf physiological traits. Plant Physiology 132: 2166-2173.
Brodribb TJ, Holbrook NM. 2004. Stomatal protection against hydraulic failure: a comparison of coexisting ferns and angiosperms. New Phytologist 162: 663-670.
Brodribb TJ, McAdam SAM. 2011. Passive origins of stomatal control. Science 331: 582-585.
Brodribb TJ, McAdam SAM, Carins Murphy MR. 2017. Xylem and stomata are coordinated through time and space. Plant, Cell & Environment. 40: 872-880.
Brodribb TJ, McAdam SAM, Jordan GJ, Martins SCV. 2014. Conifer species adapt to low-rainfall climates by following one of two divergent pathways. Proceedings of the National Academy of Sciences, USA 111: 14489-14493.
Brodribb TJ, Skelton RP, McAdam SAM, Bienaimé D, Lucani CJ, Marmottant P. 2016b. Visual quantification of embolism reveals leaf vulnerability to hydraulic failure. New Phytologist 209: 1403-1409.
Brulé V, Rafsanjani A, Asgari M, Western TL, Pasini D. 2019. Three-dimensional functional gradients direct stem curling in the resurrection plant Selaginella lepidophylla. Journal of the Royal Society Interface 16: 20190454.
Buck WR, Lucansky TW. 1976. An anatomical and morphological comparison of Selaginella apoda and Selaginella ludoviciana. Bulletin of the Torrey Botanical Club 103: 9-16.
Bujan J, Yanoviak SP, Kaspari M. 2016. Desiccation resistance in tropical insects: causes and mechanisms underlying variability in a Panama ant community. Ecology and Evolution 6: 6282-6291.
Caffall KH, Mohnen D. 2009. The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydrate Research 344: 1879-1900.
Campany CE, Martin L, Watkins JE. 2019. Convergence of ecophysiological traits drives floristic composition of early lineage vascular plants in a tropical forest floor. Annals of Botany 123: 793-803.
Cardoso AA, Batz TA, McAdam SAM. 2020. Xylem embolism resistance determines leaf mortality during drought in Persea americana. Plant Physiology 182: 547-554.
Cardoso AA, Brodribb TJ, Lucani CJ, DaMatta FM, McAdam SAM. 2018. Coordinated plasticity maintains hydraulic safety in sunflower leaves. Plant, Cell & Environment 41: 2567-2576.
Cardoso AA, McAdam SAM. 2019. Misleading conclusions from exogenous ABA application: a cautionary tale about the evolution of stomatal responses to changes in leaf water status. Plant Signaling and Behavior 14: 1610307.
Cardoso AA, Randall JM, McAdam SAM. 2019. Hydraulics regulate stomatal responses to changes in leaf water status in the fern Athyrium filix-femina. Plant Physiology 179: 533-543.
Choat B, Badel E, Burlett R, Delzon S, Cochard H, Jansen S. 2016. Noninvasive measurement of vulnerability to drought-induced embolism by x-ray microtomography. Plant Physiology 170: 273-282.
Choat B, Jansen S, Brodribb TJ, Cochard H, Delzon S, Bhaskar R, Bucci SJ, Feild TS, Gleason SM, Hacke UG et al. 2012. Global convergence in the vulnerability of forests to drought. Nature 491: 752-755.
Considine JA, Knox RB. 1979. Development and histochemistry of the cells, cell walls, and cuticle of the dermal system of fruit of the grape, Vitis vinifera L. Protoplasma 99: 347-365.
Creek D, Lamarque LJ, Torres-Ruiz JM, Parise C, Burlett R, Tissue DT, Delzon S. 2019. Xylem embolism in leaves does not occur with open stomata: evidence from direct observations using the optical visualization technique. Journal of Experimental Botany 71: 1151-1159.
Cuneo IF, Barrios-Masias F, Knipfer T, Uretsky J, Reyes C, Lenain P, Brodersen CR, Walker MA, McElrone AJ. 2020. Differences in grapevine rootstock sensitivity and recovery from drought are linked to fine root cortical lacunae and root tip function. New Phytologist. doi: 10.1111/nph.16542.
Cuneo IF, Knipfer T, Brodersen CR, McElrone AJ. 2016. Mechanical failure of fine root cortical cells initiates plant hydraulic decline during drought. Plant Physiology 172: 1669-1678.
de Oliveira DC, Magalhães TA, Ferreira BG, Teixeira CT, Formiga AT, Fernandes GW, Isaias RMdS. 2014. Variation in the degree of pectin methylesterification during the development of Baccharis dracunculifolia kidney-shaped gall. PLoS ONE 9: e94588.
Deans RM, Brodribb TJ, Mcadam SAM. 2017. An integrated hydraulic-hormonal model of conifer stomata predicts water stress dynamics. Plant Physiology 174: 478-486.
Duerden H. 1934. On the occurrence of vessels in Selaginella. Annals of Botany 48: 459-465.
Duursma RA, Blackman CJ, Lopéz R, Martin-StPaul NK, Cochard H, Medlyn BE. 2018. On the minimum leaf conductance: its role in models of plant water use, and ecological and environmental controls. New Phytologist 221: 693-705.
Franks PJ, Farquhar GD. 2007. The mechanical diversity of stomata and its significance in gas-exchange control. Plant Physiology 143: 78-87.
Gola EM, Jernstedt JA. 2016. Vascular structure contributes to shoot sectoriality in Selaginella kraussiana. Acta Societatis Botanicorum Poloniae 85: 1-12.
Henry C, John GP, Pan R, Bartlett MK, Fletcher LR, Scoffoni C, Sack L. 2019. A stomatal safety-efficiency trade-off constrains responses to leaf dehydration. Nature Communications 10: 3398.
Holmlund HI, Pratt RB, Jacobsen AL, Davis SD, Pittermann J. 2019. High-resolution computed tomography reveals dynamics of desiccation and rehydration in fern petioles of a desiccation-tolerant fern. New Phytologist 224: 97-105.
Kaack L, Altaner C, Carmesin C, Diaz A, Holler M, Kranz C, Neusser G, Odstrcil M, Schenk HJ, Schmidt V et al. 2019. Function and three-dimensional structure of intervessel pit membranes in angiosperms: a review. IAWA Journal 40: 673-702.
Kidston R, Lang WH. 1920. On Old Red Sandstone plants showing structure, from the Rhynie Chert Bed, Aberdeenshire: Part III. Asteroxylon mackiei, Kidston and Lang. Royal Society of Edinburgh Transactions 52: 643-680.
King A, Guignot N, Zerbino P, Boulard E, Desjardins K, Bordessoule M, Leclerq N, Le S, Renaud G, Cerato M et al. 2016. Tomography and imaging at the PSICHE beam line of the SOLEIL synchrotron. Review of Scientific Instruments 87: 093704.
Klaus KV, Schulz C, Bauer DS, Stützel T. 2017. Historical biogeography of the ancient lycophyte genus Selaginella: early adaptation to xeric habitats on Pangea. Cladistics 33: 469-480.
Leroux O, Sørensen I, Marcus SE, Viane RLL, Willats WGT, Knox JP. 2015. Antibody-based screening of cell wall matrix glycans in ferns reveals taxon, tissue and cell-type specific distribution patterns. BMC Plant Biology 15: 56.
Li S, Lens F, Espino S, Karimi Z, Klepsch M, Schenk HJ, Schmitt M, Schuldt B, Jansen S. 2016. Intervessel pit membrane thickness as a key determinant of embolism resistance in angiosperm xylem. IAWA Journal 37: 152-171.
Lima TRA, Carvalho ECD, Martins FR, Oliveira RS, Miranda RS, Muller CS, Pereira L, Bittencourt PRL, Sobczak JCMSM, Gomes-Filho RCC et al. 2018. Lignin composition is related to xylem embolism resistance and leaf life span in trees in a tropical semiarid climate. New Phytologist 219: 1252-1262.
Martin-StPaul N, Delzon S, Cochard H. 2017. Plant resistance to drought depends on timely stomatal closure. Ecology Letters 20: 1437-1447.
McAdam SAM. 2015. Physicochemical quantification of abscisic acid levels in plant tissues with an added internal standard by ultra-performance liquid chromatography. Bio-protocol 5: 1-13.
McAdam SAM, Brodribb TJ. 2012. Fern and lycophyte guard cells do not respond to endogenous abscisic acid. Plant Cell 24: 1510-1521.
McAdam SAM, Brodribb TJ. 2013. Ancestral stomatal control results in a canalization of fern and lycophyte adaptation to drought. New Phytologist 198: 429-441.
McElwain JC. 2011. Ferns: a xylem success story. New Phytologist 192: 307-310.
McLean B, Juniper BE. 1979. The fine structure and development of the trabeculae and the trabecular ring in Selaginella kraussiana. Planta 145: 443-448.
Mickel JT, Hellwig RL. 1969. Actino-plectostely, a complex new stelar pattern in Selaginella. American Fern Journal 59: 123-134.
Mirone A, Brun E, Gouillart E, Tafforeau P, Kieffer J. 2014. The PyHST2 hybrid distributed code for high speed tomographic reconstruction with interaction reconstruction and a priori knowledge capabilities. Nuclear Instruments and Methods in Physics Research Section B: Beam Interactions with Materials and Atoms 324: 41-48.
Motzer T, Munz N, Küppers M, Schmitt D, Anhuf D. 2005. Stomatal conductance, transpiration and sap flow of tropical montane rainforest trees in southern Ecuadorian Andes. Tree Physiology 25: 1283-1293.
Oliver MJ, Tuba Z, Brent DM. 2000. The evolution of vegetative desiccation tolerance in land plants. Plant Ecology 151: 85-100.
Paganin D, Mayon SC, Gureyev TE, Miller PR, Wilkins SW. 2002. Simultaneous phase and amplitude extraction from a single defocused image of a homogeneous object. Journal of Microscopy 206: 33-40.
Pampurova S, Van Dijck P. 2014. The desiccation tolerant secrets of Selaginella lepidophylla: What we have learned so far? Plant Physiology and Biochemistry 80: 285-290.
Petruzzellis F, Pagliarani C, Savi T, Losso A, Cavalletto S, Tromba G, Dullin C, Bär A, Ganthaler A, Miotto A et al. 2018. The pitfalls of in vivo imaging techniques: evidence for cellular damage caused by synchrotron X-ray computed micro-tomography. New Phytologist 220: 104-110.
Pittermann J, Limm E, Rico C, Christman MA. 2011. Structure-function constraints of tracheid-based xylem: a comparison of conifers and ferns. New Phytologist 192: 449-461.
Powers JS, Vargas GG, Brodribb TJ, Schwartz NB, Pérez-Aviles D, Smith-Martin CM, Becknell JM, Aureli F, Blanco R, Calderón-Morales E et al. 2020. A catastrophic tropical drought kills hydraulically vulnerable tree species. Global Change Biology 26: 3122-3133.
R Core Team. 2019. mgcv: Mixed GAM computation vehicle with automatic smoothness estimation, R v.1.8-31. Vienna, Austria: R Foundation for Statistical Computing [WWW document] URL https://cran.r-project.org/web/packages/mgcv/index.html.
Rowe NP. 1988. A herbaceous lycophyte from the Lower Carboniferous Drybrook Sandstone of the Forest of Dean, Gloucestershire. Palaeontology 31: 69-83.
Ruszala EM, Beerling DJ, Franks PJ, Chater C, Casson SA, Gray JE, Hetherington AM. 2011. Land plants acquired active stomatal control early in their evolutionary history. Current Biology 21: 1030-1035.
Sack L, Holbrook NM. 2006. Leaf hydraulics. Annual Review of Plant Biology 57: 361-381.
Schmidt AR, Regalado L, Weststrand S, Korall P, Sadowski EM, Schneider H, Jansen E, Bechteler J, Krings M, Müller P et al. 2020. Selaginella was hyperdiverse already in the Cretaceous. New Phytologist. doi: 10.1111/nph.16600.
Schneider EL, Carlquist S. 2000a. SEM studies on vessels of the homophyllous species of Selaginella. International Journal of Plant Sciences 161: 967-974.
Schneider EL, Carlquist S. 2000b. SEM studies on the vessels of heterophyllous species of Selaginella. International Journal of Plant Sciences 127: 263-270.
Schneider H, Schuettpelz E, Pryer KM, Cranfill R, Magallón S, Lupia R. 2004. Ferns diversified in the shadow of angiosperms. Nature 428: 553-557.
Scholz A, Klepsch MM, Zohreh K, Jansen S. 2013. How to quantify conduits in wood? Frontiers in Plant Science 4: 56.
Schulz C, Little DP, Stevenson DW, Bauer D, Moloney C, Stützel T. 2010. An overview of the morphology, anatomy, and life cycle of a new model species: the lycophyte Selaginella apoda (L.) spring. International Journal of Plant Sciences 171: 693-712.
Schuster AC, Burghardt M, Riederer M. 2017. The ecophysiology of leaf cuticular transpiration: are cuticular water permeabilities adapted to ecological conditions? Journal of Experimental Botany 68: 5271-5279.
Scoffoni C, Albuquerque C, Brodersen C, Townes SV, John GP, Bartlett MK, Buckley TN, McElrone AJ, Sack L. 2017. Outside-xylem vulnerability, not xylem embolism, controls leaf hydraulic decline during dehydration. Plant Physiology 173: 1197-1210.
Soni DK, Ranjan S, Singh R, Khare PB, Pathre UV, Shirke PA. 2012. Photosynthetic characteristics and the response of stomata to environmental determinants and ABA in Selaginella bryopteris, a resurrection spike moss species. Plant Science 191-192: 43-52.
Sterling C. 1970. Crystal-structure of ruthenium red and stereochemistry of its pectic stain. American Journal of Botany 57: 172-175.
Stewart W, Rothwell G. 2010. Paleobotany and the evolution of plants. Cambridge, UK: Cambridge University Press.
Trueba S, Pouteau R, Lens F, Feild TS, Isnard S, Olson ME, Delzon S. 2017. Vulnerability to xylem embolism as a major correlate of the environmental distribution of rain forest species on a tropical island. Plant, Cell & Environment 40: 277-289.
Tyree MT, Hammel HT. 1972. The measurement of the turgor pressure and the water relations of plants by the pressure-bomb technique. Journal of Experimental Botany 23: 267-282.
Tyree MT, Sperry JS. 1989. Vulnerability of xylem to cavitation and embolism. Annual Review of Plant Physiology and Plant Molecular Biology 40: 19-38.
Urli M, Porté AJ, Cochard H, Guengant Y, Burlett R, Delzon S. 2013. Xylem embolism threshold for catastrophic hydraulic failure in angiosperm trees. Tree Physiology 33: 672-683.
Ursache R, Andersen TG, Marhavý P, Geldner N. 2018. A protocol for combining fluorescent proteins with histological stains for diverse cell wall components. The Plant Journal 93: 399-412.
van Doorn WG, Hiemstra T, Fanourakis D. 2011. Hydrogel regulation of xylem water flow: an alternative hypothesis. Plant Physiology 157: 1642-1649.
Vanburen R, Wai CM, Ou S, Pardo J, Bryant D, Jiang N, Mockler TC, Edger P, Michael TP. 2018. Extreme haplotype variation in the desiccation-tolerant clubmoss Selaginella lepidophylla. Nature Communications 9: 13.
Voragen AGJ, Coenen G-J, Verhoef RP, Schols HA. 2009. Pectin, a versatile polysaccharide present in plant cell walls. Structural Chemistry 20: 263.
Weis KG, Polito VS, Labavitch JM. 1988. Microfluorometry of pectic materials in the dehiscence zone of almond (Prunus dulcis [Mill.] DA Webb) fruits. Journal of Histochemistry and Cytochemistry 36: 1037-1041.
Weng J-K, Akiyama T, Bonawitz ND, Li X, Ralph J, Chapple C. 2010. Convergent evolution of syringyl lignin biosynthesis via distinct pathways in the lycophyte Selaginella and flowering plants. Plant Cell 22: 1033-1045.
Weng J, Akiyama T, Ralph J, Chapple C. 2011. Independent recruitment of an O-methyltransferase for syringyl lignin biosynthesis in Selaginella moellendorffii. Plant Cell 23: 2708-2724.
Weng J, Li X, Stout J, Chapple C. 2008. Independent origins of syringyl lignin in vascular plants. Proceedings of the National Academy of Sciences, USA 105: 7887-7892.
Zhang Y, Carmesin C, Kaack L, Klepsch MM, Kotowska M, Matei T, Schenk HJ, Weber M, Walther P, Schmidt V et al. 2020. High porosity with tiny pore constrictions and unbending pathways characterise the 3D structure of intervessel pit membranes in angiosperm xylem. Plant, Cell & Environment 43: 116-130.
Zhang Y, Klepsch MM, Jansen S. 2017. Bordered pits in xylem of vesselless angiosperms and their possible misinterpretation as perforation plates. Plant, Cell & Environment 40: 2133-2146.
Zhou XM, Rothfels CJ, Zhang L, He ZR, Le Péchon T, He H, Lu NT, Knapp R, Lorence D, He XJ et al. 2016. A large-scale phylogeny of the lycophyte genus Selaginella (Selaginellaceae: Lycopodiopsida) based on plastid and nuclear loci. Cladistics 32: 360-389.
Ziegler C, Coste S, Stahl C, Delzon S, Levionnois S, Cazal J, Cochard H, Esquivel-Muelbert A, Goret J-Y, Heuret P et al. 2019. Large hydraulic safety margins protect Neotropical canopy rainforest tree species against hydraulic failure during drought. Annals of Forest Science 76: 115.

Auteurs

Amanda A Cardoso (AA)

Purdue Center for Plant Biology, Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN, 47907, USA.

Dominik Visel (D)

Institute of Systematic Botany and Ecology, Ulm University, Albert-Einstein-Allee 11, Ulm, 89081, Germany.

Cade N Kane (CN)

Purdue Center for Plant Biology, Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN, 47907, USA.

Timothy A Batz (TA)

Purdue Center for Plant Biology, Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN, 47907, USA.

Clara García Sánchez (C)

Institute of Systematic Botany and Ecology, Ulm University, Albert-Einstein-Allee 11, Ulm, 89081, Germany.

Lucian Kaack (L)

Institute of Systematic Botany and Ecology, Ulm University, Albert-Einstein-Allee 11, Ulm, 89081, Germany.

Laurent J Lamarque (LJ)

INRAE, BIOGECO, University of Bordeaux, Pessac, 33615, France.

Yael Wagner (Y)

Department of Plant & Environmental Sciences, Weizmann Institute of Science, Rehovot, 76100, Israel.

Andrew King (A)

Synchrotron Source Optimisée de Lumière d'Energie Intermédiaire du LURE, L'Orme de Merisiers, Saint Aubin-BP48, Gif-sur-Yvette Cedex, France.

José M Torres-Ruiz (JM)

INRAE, PIAF, Université Clermont-Auvergne, Clermont-Ferrand, 63000, France.

Déborah Corso (D)

INRAE, BIOGECO, University of Bordeaux, Pessac, 33615, France.

Régis Burlett (R)

INRAE, BIOGECO, University of Bordeaux, Pessac, 33615, France.

Eric Badel (E)

INRAE, PIAF, Université Clermont-Auvergne, Clermont-Ferrand, 63000, France.

Hervé Cochard (H)

INRAE, PIAF, Université Clermont-Auvergne, Clermont-Ferrand, 63000, France.

Sylvain Delzon (S)

INRAE, BIOGECO, University of Bordeaux, Pessac, 33615, France.

Steven Jansen (S)

Institute of Systematic Botany and Ecology, Ulm University, Albert-Einstein-Allee 11, Ulm, 89081, Germany.

Scott A M McAdam (SAM)

Purdue Center for Plant Biology, Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN, 47907, USA.

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