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Bundle sheath extensions are linked to water relations but not to mechanical and structural properties of leaves

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Abstract

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Bundle sheath extensions (BSEs) are linked to leaf gas exchange and drought tolerance but not to leaf mechanical and structural properties across species from a cool temperate forest.

Abstract

Bundle sheath extensions (BSEs) account for the physiological differences between heterobaric and homobaric species. The boundary that divides these two groups, however, has been elusive; and the contribution of BSEs to leaf mechanical properties is not yet fully understood. Here, we quantified the density of BSEs (D BSE) and evaluated whether it contributes to the leaf mechanical properties and water relations across species, and if so, how it does this. We studied 15 woody species that had different leaf functional types and D BSE from a cool temperate forest. We quantified four leaf mechanical properties, eight traits related to water relations, and seven structural traits of the leaf and stem. Density of BSEs was independent of leaf mechanical and structural properties and C/N concentration across species. Conversely, D BSE was correlated positively with stomatal conductance, and negatively with leaf water potential at turgor loss and midday water potential across species. Our results demonstrate that BSEs are associated with key leaf physiological properties, including gas exchange and drought tolerance, and are independent of leaf mechanical and structural properties. Thus, variation in D BSE could provide a basis for explaining the ecological strategies and distributions of different tree species.

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References

  • Ackerly DD (2000) Taxon sampling, correlated evolution, and independent contrasts. Evol Int J org Evol 54:1480–1492

    Article  CAS  Google Scholar 

  • Ando M, Noborio H, Kubota J, Kawanabe S (1989) Analysis of the meteorological data in Ashiu (1) Compare the observation data of Jimusho at about 360 m and Chojidani at 640 m above sea level. Bull Kyoto Univ For 61:25–45 (in Japanese)

    Google Scholar 

  • Anten NP, Alcala-Herrera R, Schieving F, Onoda Y (2010) Wind and mechanical stimuli differentially affect leaf traits in Plantago major. New Phytol 188:554–564

    Article  PubMed  Google Scholar 

  • Balsamo RA, Bauer AM, Davis SD, Rice BM (2003) Leaf biomechanics, morphology, and anatomy of the deciduous mesophyte Prunus serrulata (Rosaceae) and the evergreen sclerophyllous shrub Heteromeles arbutifolia (Rosaceae). Am J Bot 90:72–77

    Article  PubMed  Google Scholar 

  • Balsamo RA, Willigen CV, Bauer AM, Farrant J (2006) Drought tolerance of selected Eragrostis species correlates with leaf tensile properties. Ann Bot 97:985–991

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bates LM, Hall AE (1982) Diurnal and seasonal responses of stomatal conductance for cowpea plants subjected to different levels of environmental drought. Oecologia 54:304–308

    Article  CAS  PubMed  Google Scholar 

  • Beyschlag W, Pfanz H (1990) A fast method to detect the occurrence of nonhomogeneous distribution of stomatal aperture in heterobaric plant leaves: experiments with Arbutus-Unedo L during the diurnal course. Oecologia 82:52–55

    Article  CAS  PubMed  Google Scholar 

  • Boyce CK, Brodribb TJ, Feild TS, Zwieniecki MA (2009) Angiosperm leaf vein evolution was physiologically and environmentally transformative. Proc R Soc B 276:1771–1776

    Article  PubMed  PubMed Central  Google Scholar 

  • Brodribb TJ, Holbrook MN (2004) Stomatal protection against hydraulic failure: a comparison of coexisting ferns and angiosperms. New Phytolo 162:663–670

    Article  Google Scholar 

  • Brodribb TJ, Holbrook NM, Edwards EJ, Gutierrez MV (2003) Relations between stomatal closure, leaf turgor and xylem vulnerability in eight tropical dry forest trees. Plant Cell Environ 26:443–450

    Article  Google Scholar 

  • Brodribb TJ, Feild TS, Jordan GJ (2007) Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiol 144:1890–1898

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brodribb TJ, Jordan GJ, Carpenter RJ (2013) Unified changes in cell size permit coordinated leaf evolution. New Phytol 199:559–570

    Article  PubMed  Google Scholar 

  • Buckley TN, Sack L, Gilbert ME (2011) The role of bundle sheath extensions and life form in stomatal responses to leaf water status. Plant Physiol 156:962–973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choong M, Lucas P, Ong J, Pereira B, Tan H, Turner I (1992) Leaf fracture toughness and sclerophylly: their correlations and ecological implications. New Phytol 121:597–610

    Article  Google Scholar 

  • Coley PD (1983) Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecol Monogr 53:209–234

    Article  Google Scholar 

  • Esau K (1977) Anatomy of seed plants, 2nd edn. John Wiley, New York

    Google Scholar 

  • Escoto-Rodríguez M, Facelli JM, Watling JR (2014) Do wide crowns in arid woodland trees reflect hydraulic limitation and reduction of self-shading? Funct Plant Biol 41:1221–1229

    Article  Google Scholar 

  • Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon Isotope Discrimination and Photosynthesis. Annu Rev Plant Biol 40:503–537

    Article  CAS  Google Scholar 

  • Group for the Study on Ecology of Natural Forest (1972) Vegetation of the natural forest of Kyoto University Forest in Ashiu. Bull Kyoto Univ For 43:33–52 (in Japanese)

    Google Scholar 

  • Hacke UG, Sperry JS (2001) Functional and ecological xylem anatomy. Perspect Plant Ecol Evol Syst 4:97–115

    Article  Google Scholar 

  • Hacke UG, Sperry JS, Pockman WT, Davis SD, McCulloh KA (2001) Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure. Oecologia 126:457–461

    Article  PubMed  Google Scholar 

  • Hao GY, Sack L, Wang AY, Cao KF, Goldstein G (2010) Differentiation of leaf water flux and drought tolerance traits in hemiepiphytic and non-hemiepiphytic Ficus tree species. Funct Ecol 24:731–740

    Article  Google Scholar 

  • Inoue Y, Kenzo T, Tanaka-Oda A, Yoneyama Y, Ichie T (2015) Leaf water use in heterobaric and homobaric leafed canopy tree species in a Malaysian tropical rain forest. Photosynthetica 53:177–186

    Article  CAS  Google Scholar 

  • Jacobsen AL, Pratt RB, Ewers FW, Davis SD (2007) Cavitation resistance among 26 chaparral species of southern California. Ecol Monogr 77:99–115

    Article  Google Scholar 

  • Jones MB, Muthuri FM (1984) The diurnal course of plant water potential, stomatal conductance and transpiration in a papyrus (Cyperus Papyrus L) canopy. Oecologia 63:252–255

    Article  CAS  PubMed  Google Scholar 

  • Kamakura M, Kosugi Y, Takanashi S, Matsumoto K, Okumura M, Philip E (2011) Patchy stomatal behavior during midday depression of leaf CO2 exchange in tropical trees. Tree Physiol 31:160–168

    Article  PubMed  Google Scholar 

  • Karabourniotis G, Bornman JF, Nikolopoulos D (2000) A possible optical role of the bundle sheath extensions of the heterobaric leaves of Vitis vinifera and Quercus coccifera. Plant Cell Environ 23:423–430

    Article  Google Scholar 

  • Kashimura S, Hiromi T, Ninomiya I (2000) The leaf anatomical structure of broadleaf plant. Homobaric leaf and heterobaric leaf. Bull Ehime Univ For 38:23–36 (in Japanese)

    Google Scholar 

  • Kenzo T, Ichie T, Watanabe Y, Hiromi T (2007) Ecological distribution of homobaric and heterobaric leaves in tree species of Malaysian lowland tropical rainforest. Am J Bot 94:764–775

    Article  PubMed  Google Scholar 

  • Kitajima K, Poorter L (2010) Tissue-level leaf toughness, but not lamina thickness, predicts sapling leaf lifespan and shade tolerance of tropical tree species. New Phytol 186:708–721

    Article  PubMed  Google Scholar 

  • Kitajima K, Llorens AM, Stefanescu C, Timchenko MV, Lucas PW, Wright SJ (2012) How cellulose-based leaf toughness and lamina density contribute to long leaf lifespans of shade-tolerant species. New Phytol 195:640–652

    Article  PubMed  Google Scholar 

  • Koch GW, Sillett SC, Jennings GM, Davis SD (2004) The limits to tree height. Nature 428:851–854

    Article  CAS  PubMed  Google Scholar 

  • Lawson T, Morison J (2006) Visualising patterns of CO2 diffusion in leaves. New Phytol 169:641–643

    Article  PubMed  Google Scholar 

  • Liakoura V, Fotelli MN, Rennenberg H, Karabourniotis G (2009) Should structure-function relations be considered separately for homobaric vs. heterobaric leaves? Am J Bot 96:612–619

    Article  PubMed  Google Scholar 

  • Lucas PW, Turner IM, Dominy NJ, Yamashita N (2000) Mechanical defences to herbivory. Ann Bot 86:913–920

    Article  Google Scholar 

  • Lynch DJ, McInerney FA, Kouwenberg LL, Gonzalez-Meler MA (2012) Plasticity in bundle sheath extensions of heterobaric leaves. Am J Bot 99:1197–1206

    Article  PubMed  Google Scholar 

  • McElwain JC, Yiotis C, Lawson T (2016) Using modern plant trait relationships between observed and theoretical maximum stomatal conductance and vein density to examine patterns of plant macroevolution. New Phytol 209:94–103

    Article  CAS  PubMed  Google Scholar 

  • Morison J, Lawson T (2007) Does lateral gas diffusion in leaves matter? Plant Cell Environ 30:1072–1085

    Article  CAS  PubMed  Google Scholar 

  • Mott KA, Shope JC, Buckley TN (1999) Effects of humidity on light-induced stomatal opening: evidence for hydraulic coupling among stomata. J Exp Bot 50:1207–1213

    Article  CAS  Google Scholar 

  • Nikolopoulos D, Liakopoulos G, Drossopoulos I, Karabourniotis G (2002) The relationship between anatomy and photosynthetic performance of heterobaric leaves. Plant Physiol 129:235–243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Onoda Y, Westoby M, Adler PB, Choong AM, Clissold FJ, Cornelissen JH, Diaz S, Dominy NJ, Elgart A, Enrico L et al (2011) Global patterns of leaf mechanical properties. Ecol Lett 14:301–312

    Article  PubMed  Google Scholar 

  • Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290

    Article  CAS  PubMed  Google Scholar 

  • Pieruschka R, Schurr U, Jensen M, Wolff WF, Jahnke S (2006) Lateral diffusion of CO2 from shaded to illuminated leaf parts affects photosynthesis inside homobaric leaves. New Phytol 169:779–787

    Article  PubMed  Google Scholar 

  • Pieruschka R, Chavarria-Krauser A, Schurr U, Jahnke S (2010) Photosynthesis in lightfleck areas of homobaric and heterobaric leaves. J Exp Bot 61:1031–1039

    Article  CAS  PubMed  Google Scholar 

  • R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rasband WS (2008) ImageJ. U.S. National Institutes of Health, Bethesda, MD

    Google Scholar 

  • Read J, Stokes A (2006) Plant biomechanics in an ecological context. Am J Bot 93:1546–1565

    Article  PubMed  Google Scholar 

  • Reich PB (2014) The world-wide ‘fast-slow’ plant economics spectrum: a traits manifesto. J Ecol 102:275–301

    Article  Google Scholar 

  • Sack L, Frole K (2006) Leaf structural diversity is related to hydraulic capacity in tropical rain forest trees. Ecology 87:483–491

    Article  PubMed  Google Scholar 

  • Sack L, Holbrook NM (2006) Leaf hydraulics. Annu Rev Plant Biol 57:361–381

    Article  CAS  PubMed  Google Scholar 

  • Schulte PJ, Hinckley TM (1985) A comparison of pressure-volume curve data analysis techniques. J Exp Bot 36:1590–1602

    Article  Google Scholar 

  • Seibt U, Rajabi A, Griffiths H, Berry JA (2008) Carbon isotopes and water use efficiency: sense and sensitivity. Oecologia 155:441–454

    Article  PubMed  Google Scholar 

  • Sommerville KE, Sack L, Ball MC (2012) Hydraulic conductance of Acacia phyllodes (foliage) is driven by primary nerve (vein) conductance and density. Plant Cell Environ 35:158–168

    Article  PubMed  Google Scholar 

  • Takanashi S, Kosugi Y, Matsuo N, Tani M, Ohte N (2006) Patchy stomatal behavior in broad-leaved trees grown in different habitats. Tree Physiol 26:1565–1578

    Article  PubMed  Google Scholar 

  • Terashima I (1992) Anatomy of nonuniform leaf photosynthesis. Photosynth Res 31:195–212

    Article  CAS  PubMed  Google Scholar 

  • Tyree MT, Hammel HT (1972) The measurement of the turgor pressure and the water relations of plants by the pressure-bomb technique. J Exp Bot 23:267–282

    Article  Google Scholar 

  • Webb CO, Donoghue MJ (2005) Phylomatic: tree assembly for applied phylogenetics. Mol Ecol Notes 5:181–183

    Article  Google Scholar 

  • West JD, Peak D, Peterson JQ, Mott KA (2005) Dynamics of stomatal patches for a single surface of Xanthium strumarium L. leaves observed with fluorescence and thermal images. Plant Cell Environ 28:633–641

    Article  Google Scholar 

  • Westbrook JW, Kitajima K, Burleigh JG, Kress WJ, Erickson DL, Wright SJ (2011) What makes a leaf tough? Patterns of correlated evolution between leaf toughness traits and demographic rates among 197 shade-tolerant woody species in a neotropical forest. Am Nat 177:800–811

    Article  PubMed  Google Scholar 

  • Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827

    Article  CAS  PubMed  Google Scholar 

  • Wylie RB (1943) The role of the epidermis in foliar organization and its relations to the minor venation. Am J Bot 30:273–280

    Article  Google Scholar 

  • Wylie RB (1952) The bundle sheath extension in leaves of dicotyledons. Am J Bot 39:645–651

    Article  Google Scholar 

  • Zanne AE, Tank DC, Cornwell WK, Eastman JM, Smith SA, FitzJohn RG, McGlinn DJ, O’Meara BC, Moles AT, Reich PB et al (2014) Three keys to the radiation of angiosperms into freezing environments. Nature 506:89–92

    Article  CAS  PubMed  Google Scholar 

  • Zsogon A, Negrini AC, Peres LE, Nguyen HT, Ball MC (2015) A mutation that eliminates bundle sheath extensions reduces leaf hydraulic conductance, stomatal conductance and assimilation rates in tomato (Solanum lycopersicum). New Phytol 205:618–626

    Article  PubMed  Google Scholar 

  • Zwieniecki MA, Brodribb TJ, Holbrook NM (2007) Hydraulic design of leaves: insights from rehydration kinetics. Plant Cell Environ 30:910–921

    Article  PubMed  Google Scholar 

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Acknowledgements

Drs. A. Osawa, M. Dannoura, and Y. Onoda provided valuable advice on advancing this research. Dr. E. Beck and two anonymous reviewers made valuable suggestions to improve the manuscript. We were assisted in trait measurement by A. Abe, T. Natsume, and T. Hayashi. Ashiu Forest Research Station (FSERC) permitted us to collect tree samples. Dr. M. Nakamura helped with the tensile testing. Analysis was conducted using the Isotope Ratio Mass Spectrometer at the Cooperative Research Facilities of the Center for Ecological Research, Kyoto University, Japan.

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  1. Graduate School of Agriculture, Kyoto University, Kitashirakawa Oiwake-cho, Sakyo-ku, Kyoto, 606-8502, Japan

    Kiyosada Kawai, Rintaro Miyoshi & Naoki Okada

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  1. Kiyosada Kawai
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  2. Rintaro Miyoshi
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  3. Naoki Okada
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Correspondence to Kiyosada Kawai.

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Communicated by E. Beck.

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Kawai, K., Miyoshi, R. & Okada, N. Bundle sheath extensions are linked to water relations but not to mechanical and structural properties of leaves. Trees 31, 1227–1237 (2017). https://doi.org/10.1007/s00468-017-1540-8

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