Contrasting hydraulic strategies in Salix psammophila and Caragana korshinskii in the southern Mu Us Desert, China
Tóm tắt
Salix psammophila and Caragana korshinskii are two common shrubs in the southern Mu Us Desert, China. Their hydraulic strategies for adapting to this harsh, dry desert environment are not yet clear. This study examined the hydraulic transport efficiency, vulnerability to cavitation, and daily embolism refilling in the leaves and stems of these two shrubs during the dry season. In order to gain insight into water use strategies of whole plants, other related traits were also considered, including daily changes in stomatal conductance, leaf mass per area, leaf pressure–volume parameters, wood density and the Huber value. The leaves and stems of S. psammophila had greater hydraulic efficiency, but were more vulnerable to drought-induced hydraulic dysfunction than C. korshinskii. The difference between leaf and stem water potential at 50 % loss of conductivity was 0.12 MPa for S. psammophila and 0.81 MPa for C. korshinskii. Midday stomatal conductance decreased by 74 % compared to that at 8:30 in S. psammophila, whereas no change occurred in C. korshinskii. Daily embolism and refilling occurred in the stems of S. psammophila and leaves of C. korshinskii. These results suggest that a stricter stomatal regulation, daily embolism repair in stems, and a higher stem water capacitance could be partially compensating for the greater susceptibility to xylem embolism in S. psammophila, whereas higher leaf elastic modulus, greater embolism resistance in stems, larger difference between leaf and stem hydraulic safety, and drought-induced leaf shedding in C. korshinskii were largely responsible for its more extensive distribution in arid and desert steppes.
Tài liệu tham khảo
Anderegg WR, Plavcová L, Anderegg LD, Hacke UG, Berry JA, Field CB (2013) Drought’s legacy: multiyear hydraulic deterioration underlies wisespread aspen forest die-off and portends increased future risk. Global Change Biol 37:1074–1085. doi:10.1111/gcb.12100
Bartlett MK, Scoffoni C, Sack L (2012) The determinants of leaf turgor loss point and prediction of drought tolerance of species and biomes: a global meta-analysis. Ecol Lett 15:393–405. doi:10.1111/j.1461-0248.2012.01751.x
Blackman CJ, Brodribb TJ, Jordan GJ (2010) Leaf hydraulic vulnerability is related to conduit dimensions and drought resistance across a diverse range of woody angiosperms. New Phytol 188:1113–1123. doi:10.1111/j.1469-8137.2010.03439.x
Brodersen CR, McElrone AJ (2013) Maintenance of xylem network transport capacity: a review of embolism repair in vascular plants. Front Plant Sci 4:108. doi:10.3389/fpls.2013.00108
Brodersen CR, McElrone AJ, Choat B, Matthews MA, Shackel KA (2010) The dynamics of embolism repair in xylem: in vivo visualizations using high-resolution computed tomography. Plant Physiol 154:1088–1095. doi:10.1104/pp.110.162396
Brodribb TJ, Field TS (2000) Stem hydraulic supply is linked to leaf photosynthetic capacity: evidence from New Caledonian and Tasmanian rainforests. Plant Cell Environ 23:1381–1388. doi:10.1111/pce.12182
Brodribb TJ, Holbrook NM (2003) Stomatal closure during leaf dehydration, correlation with other leaf physiological traits. Plant Physiol 132:2166–2173. doi:10.1104/pp.103.023879
Brodribb TJ, Holbrook NM (2004) Diurnal depression of leaf hydraulic conductance in a tropical tree species. Plant Cell Environ 27:820–827. doi:10.1111/j.1365-3040.2004.01188.x
Bucci SJ, Scholz FG, Goldstein G, Meinzer FC, Arce ME (2009) Soil water availability and rooting depth as determinants of hydraulic architecture of Patagonian woody species. Oecologia 160:631–641. doi:10.1007/s00442-009-1331-z
Bucci SJ, Scholz FG, Campanello PI, Montti L, Jimenez-Castillo M, Rockwell FA, Manna LL, Guerra P, Bernal PL, Troncoso O, Enricci J, Holbrook MN, Goldstein G (2012) Hydraulic differences along the water transport system of South American Nothofagus species: do leaves protect the stem functionality? Tree Physiol 32:880–892. doi:10.1093/treephys/tps054
Bucci SJ, Scholz FG, Peschiutta ML, Arias NS, Meinzer FC, Goldstein G (2013) The stem xylem of Patagonian shrubs operates far from the point of catastrophic dysfunction and is additionally protected from drought-induced embolism by leaves and roots. Plant Cell Environ 36:2163–2174. doi:10.1111/pce.12126
Cao WH, Zhang XY (1991) The secondary xylem anatomy of six desert plants of Caragana. Acta Bot Sin 33:181–187
Chen JW, Zhang Q, Li XS, Cao KF (2009) Independence of stem and leaf hydraulic traits in six Euphorbiaceae tree species with contrasting leaf phenology. Planta 230:459–468. doi:10.1007/s00425-009-0959-6
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. doi:10.1111/j.1365-3040.2005.01336.x
Choat B, Jansen S, Brodribb TJ, Cochard H, Delzon S, Bhaskar R, Bucci SJ, Feild TS, Gleason SM, Hacke UG, Jacobsen AL, Lens F, Maherali H, Martínez-Vilalta J, Mayr S, Mencuccini M, Mitchell PJ, Nardini A, Pittermann J, Pratt RB, Sperry JS, Westoby M, Wright IJ, Zanne AE (2012) Global convergence in the vulnerability of forests to drought. Nature 491:752–755. doi:10.1038/nature11688
Christensen-Dalsgaard KK, Tyree MT (2014) Frost fatigue and spring recovery of xylem vessels in three diffuse-porous trees in situ. Plant Cell Environ 37:1074–1085. doi:10.1111/pce.12216
Clearwater MJ, Goldstein G (2005) Embolism repair and long distance water transport. In: Holbrook NM, Zwieniecki MA (eds) Vasular transport in plants. Elsevier Academic Press, Burlington, pp 375–399
Cochard H, Casella E, Mencuccini M (2007) Xylem vulnerability to cavitation varies among poplar and willow clones and correlates with yield. Tree Physiol 27:1761–1767. doi:10.1093/treephys/27.12.1761
Cochard H, Badel E, Herbette S, Delzon S, Choat B, Jansen S (2013) Methods for measuring plant vulnerability to cavitation: a critical review. J Exp Bot 64:4779–4791. doi:10.1093/jxb/ert193
Davis SD, Ewers FW, Sperry JS, Portwood KA, Crocker MC, Adams GC (2002) Shoot dieback during prolonged drought in Ceanothus (Rhamnaceae) chaparral of California: a possible case of hydraulic failure. Am J Bot 89:820–828. doi:10.3732/ajb.89.5.820
Delzon S, Cochard H (2014) Recent advances in tree hydraulics highlight the ecological significance of the hydraulic safety margin. New Phytol 203:355–358. doi:10.1111/nph.12798
Dong XJ, Zhang XS (2001) Some observations of the adaptations of sandy shrubs to the arid environment in the Mu Us Sandland: leaf water relations and anatomic features. J Arid Environ 48:41–48. doi:10.1006/jare.2000.0700
Fang XW, Li FM, Zhang HN, Jiang ZR (2011) The comparation of drought resistance between Caragana species (C. arborescens, C. korshinskii, C. microphylla) and two chickpea (Cicer arietinum L.) cultivars. Acta Ecol Sin 31:2437–2443
Fang XW, Turner NC, Xu DH, Jin Y, He H, Li FM (2013) Limits to the height growth of Caragana korshinskii resprouts. Tree Physiol 33:275–284. doi:10.1093/treephys/tpt006
Hacke UG, Sperry JS, Pockman WT, Davis SD, McCulloh KA (2001a) Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure. Oecologia 126:457–461. doi:10.1007/s004420100628
Hacke UG, Stiller V, Sperry JS, Pittermann J, McCulloh K (2001b) Cavitation fatigue: embolism and refilling cycles can weaken the cavitation resistance of xylem. Plant Physiol 125:779–786. doi:10.1104/pp.125.2.779
Hacke UG, Sperry JS, Wheeler JK, Castro L (2006) Scaling of angiosperm xylem structure with safety and efficiency. Tree Physiol 26:689–701. doi:10.1093/treephys/26.6.689
Hao GW, HoffmannWA Scholz FG, Bucci SJ, Meinzer FC, Franco AC, Cao KF, Goldstein G (2008) Stem and leaf hydraulics of congeneric tree species from adjacent tropical savanna and forest ecosystems. Oecologia 155:405–415. doi:10.1007/s00442-007-0918-5
Hartmann H, Ziegler W, Kolle O, Trumbore S (2013) Thirst beats hunger –declining hydration during drought prevents carbon starvation in Norway spruce saplings. New Phytol 200:340–349. doi:10.1111/nph.12331
Hukin D, Cochard H, Dreyer E, Thiec LD, Bogeat-Triboulot MB (2005) Cavitation vulnerability in roots and shoots: does Populus euphratica Oliv., a poplar from arid areas of Central Asia, differ from other poplar species? J Exp Bot 56:2003–2010. doi:10.1093/jxb/eri198
Jacobsen AL, Pratt RB, Davies SD, Ewers FW (2007) Cavitation resistance and seasonal hydraulics differ among three arid Californian plant communities. Plant Cell Environ 30:1599–1609. doi:10.1111/j.1365-3040.2007.01729.x
Johnson DM, McCulloh KA, Woodruff DR, Meinzer FC (2012) Hydraulic safety margins and embolism reversal in stems and leaves: why are conifers and angiosperms so different? Plant Sci 195:48–53. doi:10.1016/j.plantsci.2012.06.010
Klein T, Yakir D, Buchmann N, Grünzweig JM (2014) Towards an advanced assessment of the hydrological vulnerability of forests to climate change-induced drought. New Phytol 201:712–716. doi:10.1111/nph.12548
Knipfer T, Eustis A, Brodersen C, Walker AM, McElrone AJ (2015) Grapevine species from varied native habitats exhibit differences in embolism formation/repair associated with leaf gas exchange and root pressure. Plant Cell Environ 38:1503–1513. doi:10.1111/pce.12497
Li YY, Chen WY, Chen JC, Shi H (2016) Vulnerability to drought-induced cavitation in shoots of two typical shrubs in the southern Mu Us Sandy Land, China. J Arid Land 8:125–137. doi:10.1007/s40333-015-0056-6
Lo Gullo MA, Nardini A, Trifilo P, Salleo S (2003) Changes in leaf hydraulics and stomatal conductance following drought stress and irrigation in Ceratonia siliqua (Carob tree). Physiol Plant 117:186–194. doi:10.1034/j.1399-3054.2003.00038.x
Ma CC, Gao YB, Guo HY, Wang JL, Wu JB, Xu JS (2008) Physiological adaptations of four dominant Caragana species in the desert region of the Inner Mongolia Plateau. J Arid Environ 72:247–254. doi:10.1016/j.jaridenv.2007.05.009
Maherali H, Pockman WT, Jackson RB (2004) Adaptive variation in the vulnerability of woody plants to xylem cavitation. Ecology 85:2184–2199. doi:10.1890/02-0538
Malhado ACM, Whittaker RJ, Malhi Y, Ladle RJ, Ht Steege, Phillips O, Aragão LEOC, Baker TR, Arroyo L, Almeida S, Higuchi N, Killeen TJ, Monteagudo A, Pitman NCA, Prieto A, Salomão RP, Vásquez-Martínez R, Laurance WF, Ramírez-Angulo H (2010) Are compound leaves an adaptation to seasonal drought or to rapid growth? Evidence from the Amazon rain forest. Glob Ecol Biogeogr 19:852–862. doi:10.1111/j.1466-8238.2010.00567.x
Mayr S, Hacke U, Schmid P, Schwienbacher F, Gruber A (2006) Frost drought in conifers at the alpine timberline: xylem dysfunction and adaptations. Ecology 87:3175–3185. doi:10.1890/0012-9658
McCulloh KA, Meinzer FC (2015) Further evidence that some plants can lose and regain hydraulic function daily. Tree Physiol 35:691–693. doi:10.1093/treephys/tpv066
Meinzer FC, Johnson DM, Lachenbruch B, McCulloh KA, Woodruff DR (2009) Xylem hydraulic safety margins in woody plants: coordination of stomatal control of xylem tension with hydraulic capacitance. Funct Ecol 23:922–930. doi:10.1111/j.1365-2435.2009.01577.x
Melcher PJ, Holbrook NM, Burns MJ, Zwieniecki MA, Cobb AR, Brodribb TJ, Choat B, Sack L (2012) Measurements of stem xylem hydraulic conductivity in the laboratory and field. Methods Ecol Evol 3:685–694. doi:10.1111/j.2041-210X.2012.00204.x
Nardini A, Luglio J (2014) Leaf hydraulic capacity and drought vulnerability: possible trade-offs and correlations with climate across three major biomes. Funct Ecol 28:810–818. doi:10.1111/1365-2435.12246
Nardini A, Battistuzzo M, Savi T (2013) Shoot desiccation and hydraulic failure in temperature woody angiosperms during an extreme summer drought. New Phytol 200:322–329. doi:10.1111/nph.12288
Nolf M, Creek D, Duursma R, Holtum J, Mayr S, Choat B (2015) Stem and leaf hydraulic properties are finely coordinated in three tropical rain forest tree species. Plant Cell Environ 38:2652–2661. doi:10.1111/pce.12581
Ogasa M, Miki NH, Murakami Y, Yoshikawa K (2013) Recovery performance in xylem hydraulic conductivity is correlated with cavitation resistance for temperate diciduous tree species. Tree Physiol 33:335–344. doi:10.1093/treephys/tpt010
Pammenter NW, Vander Willigen C (1998) A mathematical and statistical analysis of the curves illustrating vulnerability of xylem to cavitation. Tree Physiol 18:589–593. doi:10.1093/treephys/18.8-9.589
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. doi:10.1104/pp.110.158824
Salleo S, Gullo M, Paoli D, Zippo M (1996) Xylem recovery from cavitation-induced embolism in young plants of Laurus nobilis: a possible mechanism. New Phytol 132:47–56. doi:10.1111/j.1469-8137.1996.tb04507.x
Salleo S, Nardini A, LoGullo MA (1997) Is sclerophylly of Mediterranean evergreens an adaptation to drought? New Phytol 135:603–612. doi:10.1046/j.1469-8137.1997.00696.x
Sangsing K, Kasemsap P, Thanisawanyangkura S, Sangkhasila K, Gohet E, Thaler P, Cochard H (2004) Xylem embolism and stomatal regulation in two rubber clones (Hevea brasiliensis Muell. Arg.). Trees 18:109–114. doi:10.1007/s00468-003-0286-7
Schulte PJ, Hinckley TM (1985) A comparison of pressure-volume curve data analysis techniques. J Exp Bot 36:1590–1602. doi:10.1093/jxb/36.10.1590
Scoffoni C, McKown AD, Rawls M, Sack L (2012) Dynamics of leaf hydraulic conductance with water status: quantification and analysis of species differences under steady state. J Exp Bot 63:643–658. doi:10.1093/jxb/err270
Sperry J (2013) Cutting-edge research or cutting-edge artifact? An overdue control experiment complicates the xylem refilling story. Plant Cell Environ 36:1916–1918. doi:10.1111/pce.12148
Sperry JS, Donnelly J, Tyree MT (1988) A method for measuring hydraulic conductivity and embolism in xylem. Plant Cell Environ 11:35–40. doi:10.1111/j.1365-3040.1988.tb01774.x
Taneda H, Sperry JS (2008) A case-study of water transport in co-occurring ring-versus diffuse-porous trees: contrasts in water-status, conducting capacity, cavitation and vessel refilling. Tree Physiol 28:1641–1651. doi:10.1093/treephys/28.11.1641
Trifilò P, Raimondo F, Lo Gullo MA, Barbera PM, Salleo S, Nardini A (2014) Relax and refill: xylem rehydration prior to hydraulic measurements favours embolism repair in stems and generates artificially low PLC values. Plant Cell Environ 37:2491–2499. doi:10.1111/pce.12313
Trifilò P, Nardini A, Lo Gullo MA, Barbera PM, Savi T, Raimondo F (2015) Diurnal changes in embolism rate in nine dry forest trees: relationships with species-specific xylem ulnerability, hydraulic strategy and wood traits. Tree Physiol 35:694–705. doi:10.1093/treephys/tpv049
Tyree MT, Ewers FW (1991) The hydraulic architecture of trees and other woody plants. New Phytol 119:345–360. doi:10.1111/j.1469-8137.1991.tb00035.x
Tyree MT, Sperry JS (1989) Vulnerability of xylem to cavitation and embolism. Annual Rev Plant Physiol Mol Bio 40:19–38. doi:10.1146/annurev.pp.40.060189.000315
Venturas MD, MacKinnon ED, Jacobsen AL, Pratt RB (2015) Excising stem samples underwater at native tension does not induce xylem cavitation. Plant Cell Environ 38:1060–1068. doi:10.1111/pce.12461
Vilagrosa A, Bellot J, Vallejo VR, Gil-Pelegrín (2003) Cavitation, stomatal conductance, and leaf dieback in seedlings of two co-occurring Mediterranean shrubs during an intense drought. J Exp Bot 54:2015–2024. doi:10.1093/jxb/erg221
Wang L, Mu Y, Zhang QF, Zhang XC (2013) Groundwater use by plants in a semi-arid coal-mining area at the Mu Us Desert frontier. Environ Earth Sci 69:1015–1024. doi:10.1007/s12665-012-2023-2
Wang RQ, Zhang LL, Zhang SX, Cai J, Tyree MT (2014) Water relations of Robinia pseudoacacia L.: do vessels cavitate and refill diurnally or are R-shaped curves invalid in Robinia? Plant Cell Environ 37:2667–2678. doi:10.1111/pce.12315
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
Wikberg J, Ögren E (2007) Variation in drought resistance, drought acclimation and water conservation in four willow cultivars used for biomass production. Tree Physiol 27:1339–1346. doi:10.1093/treephys/27.9.1339
Xu BC, Shan L (2004) A comparative study on water use characteristics and eco-adaptability of Hippophae rhamnoides and Caragana korshinskii in semi arid loess hilly-gully region. Chin J Appl Ecol 15:2025–2028
Zhang L, Wu B, Ding GD, Zhang YQ (2010) Root distribution characteristics of Salix psammophila and Caragana Korshinskii in Mu Us sandy land. J Arid Land Resour Environ 24:158–161
Zhang YJ, Meinzer FC, Qi JH, Goldstein G, Cao KF (2013) Midday stomatal conductance is more related to stem rather than leaf water status in subtropical deciduous and evergreen broadleaf trees. Plant Cell Environ 36:149–158. doi:10.1111/j.1365-3040.02563.x
Zwieniecki M, Holbrook NM (1998) Diurnal variation in xylem hydraulic conductivity in white ash (Fraxinus americana L.), red maple (Acer rubrum L.) and red spruce (Picea rubens Sarg.). Plant Cell Environ 21:1173–1180. doi:10.1046/j.1365-3040.1998.00342.x
Zwieniecki MA, Melcher PJ, Ahrens ET (2013) Analysis of spatial and temporal dynamics of xylem refilling in Acer rubrum L. using magnetic resonance imaging. Front Plant Sci 4:265. doi:10.3389/fpls.2013.00265