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Differences in drought- and freeze-induced embolisms in deciduous ring-porous plant species in Japan

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Abstract

Main conclusion

Deciduous ring-porous species in Japan shed all of their leaves under severe water stress before large vessels in earlywood are embolized, and embolization take place during winter.

Abstract

Water in deciduous ring-porous species is mainly conducted upward via large earlywood vessels of the current year. Water columns in large vessels are vulnerable to drought-induced and freeze stress-induced embolisms. Although a vulnerability curve can be created to estimate the hydraulic capacity of plants, it remains unclear why the loss of conductivity in potted plants of ring-porous species does not reach 100 % under severe drought stress. In this study, two deciduous ring-porous species in Japan (Kalopanax septemlobus and Toxicodendron trichocarpum) were used to explain the species-specific pattern in the water-conducting pathway of the stem. We monitored and visualized the spatial distribution of xylem embolisms in the stem of K. septemlobus saplings under drought stress and freeze stress using compact magnetic resonance imaging and cryo-scanning microscopy. In addition, we evaluated the water ascent in the stems of both species using a dye uptake method. Although embolisms of large vessels were observed under drought stress and in winter, all leaves were dropped to avoid fatal water loss after embolization of some large vessels. In contrast, all large vessels were embolized in winter. Larger-diameter vessels of latewood in T. trichocarpum tended to function in trees growing in the warm temperate zone. Thus, our results suggest that the unclear curve may be derived from a discrepancy between leaf water potential and actual water potential in the xylem under severe drought stress. The frequency of xylem embolisms in deciduous ring-porous species in Japan mainly depends on the number of freeze–thaw cycles.

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References

  • Bouche PS, Delzon S, Choat B, Badel E, Brodribb TJ, Burlett R, Cochard H, Charra-Vaskou K, Lavigne B, Li S, Mayr S, Morris H, Torres-Ruiz JM, Zufferey V, Jansen S (2016) Are needles of Pinus pinaster more vulnerable to xylem embolism than branches? New insights from X-ray computed tomography. Plant Cell Environ 39:860–870. doi:10.1111/pce.12680

    Article  CAS  PubMed  Google Scholar 

  • Chaney WR, Kozlowski TT (1977) Patterns of water movement in intact and excised stems of Fraxinus americana and Acer saccharum seedlings. Ann Bot 41:1093–1100

    Google Scholar 

  • Choat B, Drayton WM, Brodersen C, Matthews MA, Shackel KA, Wada H, McElrone AJ (2010) Measurement of vulnerability to water stress-induced cavitation in grapevine: a comparison of four techniques applied to a long-vesseled species. Plant Cell Environ 33:1502–1512. doi:10.1111/j.1365-3040.2010.02160.x

    PubMed  Google Scholar 

  • 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 Physiol 170:273–282. doi:10.1104/pp.15.00732

    Article  CAS  PubMed  Google Scholar 

  • Cochard H, Bréda N, Granier A, Aussenac G (1992) Vulnerability to air embolism of three European oak species (Quercus petraea (Matt) Liebl, Q. pubescens Willd, Q. robur L). Ann Sci For 49:225–233

    Article  Google Scholar 

  • Cochard H, Herbette S, Barigah T, Badel E, Ennajeh M, Vilagrosa A (2010) Does sample length influence the shape of xylem embolism vulnerability curves? A test with the Cavitron spinning technique. Plant Cell Environ 33:1543–1552. doi:10.1111/j.1365-3040.2010.02163.x

    PubMed  Google Scholar 

  • Davis SD, Sperry JS, Hacke UG (1999) The relationship between xylem conduit diameter and cavitation caused by freezing. Am J Bot 86:1367–1372

    Article  CAS  PubMed  Google Scholar 

  • Ellmore GS, Ewers FW (1986) Fluid flow in the outermost xylem increment of a ring porous tree, Ulmus americana. Am J Bot 73:1771–1774

    Article  Google Scholar 

  • Higgs KH, Wood V (1995) Drought susceptibility and xylem dysfunction in seedlings of 4 European oak species. Ann Sci For 52:507–513. doi:10.1051/forest:19950509

    Article  Google Scholar 

  • Hochberg U, Albuquerque C, Rachmilevitch S, Cochard H, David-Schwartz R, Brodersen CR, McElrone A, Windt CW (2016) Grapevine petioles are more sensitive to drought induced embolism than stems: evidence from in vivo MRI and microcomputed tomography observations of hydraulic vulnerability segmentation. Plant Cell Environ. doi:10.1111/pce.12688

    Google Scholar 

  • Kasuga J, Charrier G, Uemura M, Améglio T (2015) Characteristics of ultrasonic acoustic emissions from walnut branches during freeze–thaw-induced embolism formation. J Exp Bot 66:1965–1975. doi:10.1093/jxb/eru543

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kursar TA, Engelbrecht BMJ, Burke A, Tyree MT, El Omari B, Glraldo JP (2009) Tolerance to low leaf water status of tropical tree seedlings is related to drought performance and distribution. Funct Ecol 23:93–102. doi:10.1111/j.1365-2435.2008.01483.x

    Article  Google Scholar 

  • Li Y, Sperry JS, Taneda H, Bush SE, Hacke UG (2008) Evaluation of centrifugal methods for measuring xylem cavitation in conifers, diffuse- and ring-porous angiosperms. New Phytol 177, pp. 558–568. doi:10.1111/j.1469-8137.2007.02272.x

    PubMed  Google Scholar 

  • Lintunen A, Hölttä T, Kulmala M (2013) Anatomical regulation of ice nucleation and cavitation helps trees to survive freezing and drought stress. Sci Rep 3:2031. doi:10.1038/srep02031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin-StPaul NK, Longepierre D, Huc R, Delzon S, Burlett R, Joffre R, Rambal S, Cochard H (2014) How reliable are methods to assess xylem vulnerability to cavitation? The issue of ‘open vessel’ artifact in oaks. Tree Physiol 34:894–905. doi:10.1093/treephys/tpu059

    Article  CAS  PubMed  Google Scholar 

  • Mayr S, Cochard H, Améglio T, Kikuta SB (2007) Embolism formation during freezing in the wood of Picea abies. Plant Physiol 143:60–67. doi:10.1104/pp.106.085704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ogasa M, Miki N, Yoshikawa K (2010) Changes of hydraulic conductivity during dehydration and rehydration in Quercus serrata Thunb. and Betula platyphylla var. japonica Hara: the effect of xylem structures. Tree Physiol 30:608–617. doi:10.1093/treephys/tpq011

    Article  PubMed  Google Scholar 

  • Ogasa M, Miki NH, Okamoto M, Yamanaka N, Yoshikawa K (2014) Water loss regulation to soil drought associated with xylem vulnerability to cavitation in temperate ring-porous and diffuse-porous tree seedlings. Trees 28:461–469. doi:10.1007/s00468-013-0963-0

    Article  Google Scholar 

  • Pittermann J, Sperry J (2003) Tracheid diameter is the key trait determining the extent of freezing-induced embolism in conifers. Tree Physiol 23:907–914. doi:10.1093/treephys/23.13.907

    Article  PubMed  Google Scholar 

  • Pratt RB, Jacobsen AL, Mohla R, Ewers FW, Davis SD (2008) Linkage between water stress tolerance and life history type in seedlings of nine chaparral species (Rhamnaceae). J Ecol 96:1252–1265. doi:10.1111/j.1365-2745.2008.01428.x

    Article  Google Scholar 

  • Sano Y, Okamura Y, Utsumi Y (2005) Visualizing water-conduction pathways of living trees: selection of dyes and tissue preparation methods. Tree Physiol 25:269–275. doi:10.1093/treephys/25.3.269

    Article  PubMed  Google Scholar 

  • Sperry JS, Nichols KL, Sullivan JEM, Eastlack SE (1994) Xylem embolism in ring-porous, diffuse-porous, and coniferous trees of northern Utah and interior Alaska. Ecology 75:1736–1752. doi:10.2307/1939633

    Article  Google Scholar 

  • Torres-Ruiz JM, Cochard H, Mayr S, Beikircher B, Diaz-Espejo A, Rodriguez-Dominguez CM, Badel E, Fernández JE (2014) Vulnerability to cavitation in Olea europaea current-year shoots: further evidence of an open-vessel artifact associated with centrifuge and air-injection techniques. Phys Plant 152:465–474. doi:10.1111/ppl.12185

    Article  CAS  Google Scholar 

  • Torres-Ruiz JM, Jansen S, Choat B, McElrone AJ, Cochard H, Brodribb TJ, Badel E, Burlett R, Bouche PS, Brodersen CR, Li S, Morris H, Delzon S (2015) Direct X-ray microtomography observation confirms the induction of embolism upon xylem cutting under tension. Plant Physiol 167:40–43. doi:10.1104/pp.114.249706

    Article  CAS  PubMed  Google Scholar 

  • Tyree MT, Sperry JS (1989) Vulnerability of xylem to cavitation and embolism. Annu Rev Plant Phys Mol Biol 40:19–38. doi:10.1146/annurev.pp.40.060189.000315

    Article  Google Scholar 

  • Umebayashi T, Utsumi Y, Koga S, Inoue S, Fujikawa S, Arakawa K, Matsumura J, Oda K (2008) Conducting pathways in north temperate deciduous broadleaved trees. IAWA J 29:247–263. doi:10.1163/22941932-90000184

    Article  Google Scholar 

  • Umebayashi T, Utsumi Y, Koga S, Inoue S, Matsumura J, Oda K, Fujikawa S, Arakawa K, Otsuki K (2010) Xylem water-conducting patterns of 34 broadleaved evergreen trees in southern Japan. Trees 24:571–583. doi:10.1007/s00468-010-0428-7

    Article  Google Scholar 

  • Umebayashi T, Ogasa MY, Miki NH, Utsumi Y, Haishi T, Fukuda K (2016a) Freezing xylem conduits with liquid nitrogen creates artifactual embolisms in water-stressed broadleaf trees. Trees 30:305–316. doi:10.1007/s00468-015-1302-4

    Article  CAS  Google Scholar 

  • Umebayashi T, Morita T, Utsumi Y, Kusumoto D, Yasuda Y, Haishi T, Fukuda K (2016b) Spatial distribution of xylem embolisms in the stems of Pinus thunbergii at the threshold of fatal drought stress. Tree Physiol. doi:10.1093/treephys/tpw050

    PubMed  Google Scholar 

  • Utsumi Y, Sano Y, Ohtani J, Fujikawa S (1996) Seasonal changes in the distribution of water in the outer growth rings of Fraxinus mandshurica var. japonica: a study by cryo-scanning electron microscopy. IAWA J 17:113–124. doi:10.1163/22941932-90001439

    Article  Google Scholar 

  • Utsumi Y, Sano Y, Fujikawa S, Funada R, Ohtani J (1998) Visualization of cavitated vessels in winter and refilled vessels in spring in diffuse-porous trees by cryo-scanning electron microscopy. Plant Physiol 117:1463–1471. doi:10.1104/pp.117.4.1463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wheeler JK, Huggett BA, Tofte AN, Rockwell FE, Holbrook NM (2013) Cutting xylem under tension or supersaturated with gas can generate PLC and the appearance of rapid recovery from embolism. Plant Cell Environ 36:1938–1949. doi:10.1111/pce.12139

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by KAKENHI, Grants-in Aid for Scientific Research (A) (No. 23248022, 15H02450) from the Japan Society for the Promotion of Science (JSPS). We are grateful to Dr. Yuzou Sano and Dr. Yoko Watanabe, Hokkaido University, and Mr. Naoaki Tashiro and Dr. Susumu Inoue, Kyushu University, for useful comments and technical assistance.

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Correspondence to Toshihiro Umebayashi.

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Umebayashi, T., Utsumi, Y., Koga, S. et al. Differences in drought- and freeze-induced embolisms in deciduous ring-porous plant species in Japan. Planta 244, 753–760 (2016). https://doi.org/10.1007/s00425-016-2564-9

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