Cavitation resistance in seedless vascular plants: The structure and function of interconduit pit membranes

Plant Physiology

Volumn 165, Issue 2, 2014, Pages 895-904

  Brodersen, Craig ^a   Jansen, Steven ^b   Choat, Brendan ^c   Rico, Christopher ^d   Pittermann, Jarmila ^d  

^a Yale School of the Environment   (United States)

^b UNIVERSITY OF ULM   (Germany)

^c WESTERN SYDNEY UNIVERSITY   (Australia)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84901791326     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.226522     Document Type: Article

References (58)

1. Brodersen CR, McElrone AJ, Choat B, Lee EF, Shackel KA, Matthews MA (2013) In vivo visualizations of drought-induced embolism spread in Vitis vinifera. Plant Physiol 161: 1820-1829
2. Brodersen CR, Roark LC, Pittermann J (2012) The physiological implications of primary xylem organization in two ferns. Plant Cell Environ 35: 1898-1911
3. Brodribb TJ, Holbrook NM (2004) Stomatal protection against hydraulic failure: a comparison of co-existing ferns and angiosperms. New Phytol 162: 663-670
4. Burgess SSO, Pittermann J, Dawson TE (2006) Hydraulic efficiency and safety of branch xylem increases with height in Sequoia sempervirens (D. Don) crowns. Plant Cell Environ 29: 229-239
5. Cai J, Tyree MT (2010) The impact of vessel size on vulnerability curves: data and models for within-species variability in saplings of aspen, Populus tremuloides Michx. Plant Cell Environ 33: 1059-1069
6. Carlquist S (2009) Non-random vessel distribution in woods: patterns, modes, diversity correlations. Aliso 27: 39-58
7. Carlquist S, Schneider EL (2001) Vessels in ferns: structural, ecological, and evolutionary significance. Am J Bot 88: 1-13
8. Carlquist S, Schneider EL (2007) Tracheary elements in ferns: new techniques, observations and concepts. Am Fern J 97: 199-211
9. Choat B, Ball M, Luly J, Holtum J (2003) Pit membrane porosity and water stress-induced cavitation in four co-existing dry rainforest tree species. Plant Physiol 131: 41-48
10. Choat B, Brodie TW, Cobb AR, Zwieniecki MA, Holbrook NM (2006) Direct measurements of intervessel pit membrane hydraulic resistance in two angiosperm tree species. Am J Bot 93: 993-1000
11. Choat B, Cobb AR, Jansen S (2008) Structure and function of bordered pits: new discoveries and impacts on whole-plant hydraulic function. New Phytol 177: 608-625
12. 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
13. Choat B, Lahr EC, Melcher PJ, Zwieniecki MA, Holbrook NM (2005) The spatial pattern of air seeding thresholds in mature sugar maple trees. Plant Cell Environ 28: 1082-1089
14. Choat B, Pittermann J (2009) New insights into bordered pit structure and cavitation resistance in angiosperms and conifers. New Phytol 182: 557-560
15. Christman MA, Sperry JS, Adler FR (2009) Testing the 'rare pit' hypothesis for xylem cavitation resistance in three species of Acer. New Phytol 182: 664-674
16. Christman MA, Sperry JS, Smith DD (2011) Rare pits, large vessels and extreme vulnerability to cavitation in a ring-porous species. New Phytol 193: 713-720
17. Delzon S, Douthe C, Sala A, Cochard H (2010) Mechanism of water-stress induced cavitation in conifers: bordered pit structure and function support the hypothesis of seal capillary-seeding. Plant Cell Environ 33: 2101-2111
18. Domec JC, Lachenbruch B, Meinzer FC (2006) Bordered pit structure and function determine spatial patterns of air-seeding thresholds in xylem of Douglas-fir (Pseudotsuga menziesii; Pinaceae) trees. Am J Bot 93: 1588-1600
19. Domec JC, Lachenbruch B, Meinzer FC, Woodruff DR, Warren JM, McCulloh KA (2008) Maximum height in a conifer is associated with conflicting requirements for xylem design. Proc Natl Acad Sci USA 105: 12069-12074
20. Gibson AC, Calkin HW, Nobel PS (1985) Hydraulic conductance and xylem structure in tracheid-bearing plants. IAWA J 6: 293-302
21. Hacke UG, Jansen S (2009) Embolism resistance of three boreal conifer species varies with pit structure. New Phytol 182: 675-686
22. Hacke UG, Sperry JS, Feild TS, Sano Y, Sikkema EH, Pittermann J (2007) Water transport in vesselless angiosperms: conducting efficiency and cavitation safety. Int J Plant Sci 168: 1113-1126
23. Hacke UG, Sperry JS, Pittermann J (2000) Drought experience and cavitation resistance in six shrubs from the Great Basin, Utah. Basic Appl Ecol 1: 31-41
24. Hacke UG, Sperry JS, Wheeler JK, Castro L (2006) Scaling of angiosperm xylem structure with safety and efficiency. Tree Physiol 26: 689-701
25. Hargrave KR, Kolb KJ, Ewers FW, Davis SD (1994) Conduit diameter and drought-induced embolism in Salvia mellifera Greene (Labiatae). New Phytol 126: 695-705
26. Hubbard RM, Stiller V, Ryan MG, Sperry JS (2001) Stomatal conductance and photosynthesis vary linearly with plant hydraulic conductance in ponderosa pine. Plant Cell Environ 24: 113-121
27. Jansen S, Choat B, Pletsers A (2009) Morphological variation of intervessel pit membranes and implications to xylem function in angiosperms. Am J Bot 96: 409-419
28. Jansen S, Lamy JB, Burlett R, Cochard H, Gasson P, Delzon S (2012) Plasmodesmatal pores in the torus of bordered pit membranes affect cavitation resistance of conifer xylem. Plant Cell Environ 35: 1109-1120
29. Jarbeau JA, Ewers FW, Davis SD (1995) The mechanism of water-stressinduced embolism in two species of chaparral shrubs. Plant Cell Environ 18: 189-196
30. Lee J, Holbrook NM, Zwieniecki MA (2012) Ion induced changes in the structure of bordered pit membranes. Front Plant Sci 3: 55
31. Lens F, Sperry JS, Christman MA, Choat B, Rabaey D, Jansen S (2011) Testing hypotheses that link wood anatomy to cavitation resistance and hydraulic conductivity in the genus Acer. New Phytol 190: 709-723
32. Martínez-Vilalta J, Mencuccini M, Alvarez X, Camacho J, Loepfe L, Piñol J (2012) Spatial distribution and packing of xylem conduits. Am J Bot 99: 1189-1196
33. Mauseth JD, Fujii T (1994) Resin-casting: a method for investigating apoplastic spaces. Am J Bot 81: 104-110
34. Mayr S, Wolfschwenger M, Bauer H (2002) Winter-drought induced embolism in Norway spruce (Picea abies) at the alpine timberline. Physiol Plant 115: 74-80
35. McAdam SAM, Brodribb TJ (2013) Ancestral stomatal control results in a canalization of fern and lycophyte adaptation to drought. New Phytol 198: 429-441
36. Mencuccini M, Martinez-Vilalta J, Piñol J, Loepfe L, Burnat M, Alvarez X, Camacho J, Gil D (2010) A quantitative and statistically robust method for the determination of xylem conduit spatial distribution. Am J Bot 97: 1247-1259
37. Morrow AC, Dute RR (1998) Development and structure of pit membranes in the rhizome of the woody fern Botrychium dissectum. IAWA J 19: 429-441
38. Pesacreta TC, Groom LH, Rials TG (2005) Atomic force microscopy of the intervessel pit membrane in the stem of Sapium sebiferum (Euphorbiaceae). IAWA J 26: 397-426
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. Front Plant Sci 5: 285
40. Pittermann J, Choat B, Jansen S, Stuart SA, Lynn L, Dawson TE (2010) The relationships between xylem safety and hydraulic efficiency in the Cupressaceae: the evolution of pit membrane form and function. Plant Physiol 153: 1919-1931
41. Pittermann J, Limm E, Rico C, Christman MA (2011) Structure-function constraints of tracheid-based xylem: a comparison of conifers and ferns. New Phytol 192: 449-461
42. Pittermann J, Sperry JS, Hacke UG, Wheeler JK, Sikkema EH (2005) Torus-margo pits help conifers compete with angiosperms. Science 310: 1924
43. Pittermann J, Sperry JS, Hacke UG, Wheeler JK, Sikkema EH (2006) Intertracheid pitting and the hydraulic efficiency of conifer wood: the role of tracheid allometry and cavitation protection. Am J Bot 93: 1265-1273
44. Plavcová L, Jansen S, Klepsch M, Hacke UG (2013) Nobody's perfect: can irregularities in pit structure influence vulnerability to cavitation. Front Plant Sci 4: 453
45. Rockwell FE, Wheeler JK, Holbrook NM (2014) Cavitation and its discontents: opportunities for resolving current controversies. Plant Physiol 164: 1649-1660
46. Schenk JH, Espino S, Goedhart CM, Nordenstahl M, Martinez Cabrera HI, Jones CS (2006) Hydraulic integration and shrub growth form linked across continental aridity gradients. Proc Natl Acad Sci USA 105: 11248-11253
47. Scholz A, Rabaey D, Stein A, Cochard H, Smets E, Jansen S (2013) The evolution and function of vessel and pit characters with respect to cavitation resistance across 10 Prunus species. Tree Physiol 33: 684-694
48. Schulte PJ (2012) Computational fluid dynamics models of conifer bordered pits show how pit structure affects flow. New Phytol 193: 721-729
49. Schulte PJ, Gibson AC (1988) Hydraulic conductance and tracheid anatomy in six species of extant seed plants. Can J Bot 66: 1073-1079
50. Schulte PJ, Gibson AC, Nobel P (1987) Xylem anatomy and hydraulic conductance of Psilotum nudum. Am J Bot 74: 1438-1445
51. Schymanski SJ, Or D, Zwieniecki M (2013) Stomatal control and leaf thermal and hydraulic capacitances under rapid environmental fluctuations. PLoS ONE 8: e54231
52. Sperry JS, Hacke UG (2004) Analysis of circular bordered pit function: I. Angiosperm vessels with homogenous pit membranes. Am J Bot 91: 369-385
53. Sperry JS, Hacke UG, Pittermann J (2006) Size and function in conifer tracheids and angiosperm vessels. Am J Bot 93: 1490-1500
54. Tyree MT, Sperry JS (1988) Do woody plants operate near the point of catastrophic dysfunction caused by dynamic water stress? Answers from a model. 88: 574-580
55. Watkins JE Jr, Holbrook NM, Zwieniecki MA (2010) Hydraulic properties of fern sporophytes: consequences for ecological and evolutionary diversification. Am J Bot 97: 2007-2019
56. Wheeler JW, Sperry JS, Hacke UG, Hoang N (2005) Intervessel pitting and cavitation in woody Rosaceae and other vesseled plants: a basis for a safety vs. efficiency trade-off in xylem transport. Plant Cell Environ 28: 800-812
57. Zanne AE, Sweeney K, Sharma M, Orians CM (2006) Patterns and consequences of differential vascular sectoriality in 18 temperate tree and shrub species. Funct Ecol 20: 200-206
58. Zimmermann M, Tyree MT (2002) Xylem Structure and the Ascent of Sap. Springer-Verlag, Berlin