Comparison of xylem sap mineral concentrations between kiwifruit shoot types using spittlebugs for non-destructive sampling of sap
Katrina N. Buxton A B , Michael J. Clearwater C , K. Giles-Hansen C , E. W. Hewett A and Ian B. Ferguson BA Massey University, Private Bag 102-904, North Shore Mail Centre, Auckland, New Zealand.
B The Horticulture and Food Research Institute of New Zealand, Private Bag 92169, Auckland, New Zealand.
C The Horticulture and Food Research Institute of New Zealand, Te Puke Research Centre, RD 2, Te Puke, New Zealand.
D Corresponding author. Email: iferguson@hortresearch.co.nz
Functional Plant Biology 34(11) 1029-1037 https://doi.org/10.1071/FP07091
Submitted: 16 April 2007 Accepted: 5 September 2007 Published: 1 November 2007
Abstract
Excreta of the meadow spittlebug [Philaenus spumarius L. (Homoptera: Cercopidae)] feeding on leaves and pedicels of kiwifruit [Actinidia deliciosa (A. Chev.) C.F. Liang et A.R. Ferguson var. deliciosa ‘Hayward’] were collected from insects from two different positions in the vine: from long, non-terminating axillary shoots producing fruit that are high in Ca2+ and low in K+ and from short-terminating axillary shoots producing fruit that are low in Ca2+ and high in K+. The Ca2+, Mg2+, K+ and P concentrations in the excreta were determined, and found to be similar to those in the xylem sap. Daily and seasonal changes in xylem sap composition were compared in excreta collected from the two different shoot types. On average, Ca2+ and Mg2+ concentrations were higher and K+ and P concentrations were lower in xylem sap collected from pedicels on long, non-terminating axillary shoots than in sap collected from pedicels on short-terminating shoots. Differences in the mineral concentration between these two shoot types may therefore be due to differences in the xylem sap mineral concentration reaching the fruit. There was no measurable gradient in xylem sap composition within the parent shoots that could explain the differences between sap composition of the two axillary shoot types. Long, non-terminating shoots had higher leaf area, were more exposed, had higher stomatal conductance and rates of transpiration, and more negative leaf water potentials than short-terminating shoots. The higher xylem sap Ca2+ and Mg2+ concentrations of long shoots were therefore associated with higher rates of water transport to the long shoots. Xylem sap concentration differences between these two shoots types may have been because of differential loading or unloading of minerals between shoot types, associated with differences in transpiration rate or shoot growth rates. The higher transpiration rate of long shoots may cause phloem immobile minerals such as Ca2+ to accumulate to higher levels at cation exchange sites in the shoot apoplast, resulting in increased xylem sap concentrations arriving at the fruit.
Additional keywords: Actinidia deliciosa, calcium, fruit variability, inorganic nutrients, Philaenus spumarius, xylem sap.
Acknowledgements
We thank ZESPRI International Ltd and the Foundation for Research, Science and Technology (FRST; Contract C06X0202) for funding this research, FRST for the award of a Bright Futures Scholarship to KNB, S. Schmidt and A. Fletcher, for assistance with the method for vacuum extraction of xylem sap, and M. Malone, N. Gould and D. Logan for advice on the caging of spittlebugs and the collection of their excreta.
Andersen PC,
Brodbeck BV, Mizell RF
(1992) Feeding by the leafhopper, Homalodisca coagulata, in relation to xylem fluid chemistry and tension. Journal of Insect Physiology 38, 611–622.
| Crossref | GoogleScholarGoogle Scholar |
Atkinson CJ,
Ruiz LP, Mansfield TA
(1992) Calcium in xylem sap and the regulation of its delivery to the shoot. Journal of Experimental Botany 43, 1315–1324.
| Crossref | GoogleScholarGoogle Scholar |
Bollard EG
(1953) The use of tracheal sap in the study of apple-tree nutrition. Journal of Experimental Botany 4, 363–368.
| Crossref | GoogleScholarGoogle Scholar |
Broadley MR,
Bowen HC,
Cotterill HL,
Hammond JP,
Meacham MC,
Mead A, White PJ
(2004) Phylogenetic variation in the shoot mineral concentration of angiosperms. Journal of Experimental Botany 55, 321–336.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Brodbeck BV,
Mizell RF, Andersen PC
(1993) Physiological and behavioural adaptations of three species of leafhopper in response to the dilute nutrient content of xylem fluid. Journal of Insect Physiology 39, 73–81.
| Crossref | GoogleScholarGoogle Scholar |
Cheung WWK, Marshall AT
(1973) Water and ion regulation in cicadas in relation to xylem feeding. Journal of Insect Physiology 19, 1801–1816.
| Crossref | GoogleScholarGoogle Scholar |
Clark CJ, Smith GS
(1988) Seasonal accumulation of mineral nutrients by kiwifruit 2. Fruit. New Phytologist 108, 399–409.
| Crossref | GoogleScholarGoogle Scholar |
Clark CJ,
Smith GS, Walker GD
(1987) The form, distribution and seasonal accumulation of calcium in kiwifruit leaves. New Phytologist 105, 477–486.
| Crossref | GoogleScholarGoogle Scholar |
Dichio B,
Remorini D, Lang A
(2003) Developmental changes in xylem functionality in kiwifruit fruit: implications for fruit calcium accumulation. Acta Horticulturae 610, 191–195.
Ewers FW, Zimmerman MH
(1984a) The hydraulic architecture of balsam fir (Abies balsamaea). Physiologia Plantarum 60, 453–458.
| Crossref | GoogleScholarGoogle Scholar |
Ewers FW, Zimmerman MH
(1984b) The hydraulic architecture of eastern hemlock (Tsuga canadensis). Canadian Journal of Botany 62, 940–946.
Ferguson AR,
Eiseman JA, Leonard JA
(1983) Xylem sap from Actinidia chinensis: seasonal changes in composition. Annals of Botany 51, 823–833.
Ferguson IB, Bollard EG
(1976) The movement of calcium in woody stems. Annals of Botany 40, 1057–1065.
Ferguson IB,
Thorp TG,
Barnett AM,
Boyd LM, Triggs CM
(2003) Inorganic nutrient concentrations and physiological pitting in ‘Hayward’ kiwifruit. Journal of Horticultural Science & Biotechnology 78, 497–504.
Malone M,
Watson RJ, Pritchard J
(1999) The spittlebug Philaenus spumarius feeds from mature xylem at the full hydraulic tension of the transpiration stream. New Phytologist 143, 261–271.
| Crossref | GoogleScholarGoogle Scholar |
Malone M,
Herron M, Morales AM
(2002a) Continuous measurement of macronutrient ions in the transpiration stream of intact plants using the meadow spittlebug coupled with ion chromatography. Plant Physiology 130, 1436–1442.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Malone M,
White PJ, Morales AM
(2002b) Mobilisation of calcium in glasshouse tomato plants by localized scorching. Journal of Experimental Botany 53, 83–88.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Montanaro G,
Dichio B,
Xiloyannis C, Celano G
(2006) Light influences transpiration and calcium accumulation in fruit of kiwifruit plants (Actinidia deliciosa var. deliciosa). Plant Science 170, 520–527.
| Crossref | GoogleScholarGoogle Scholar |
Pate JS,
Woodall G,
Jeschke WD, Stewart GR
(1994) Root xylem transport of amino acids in the root hemiparasitic shrub Olax phyllanthi (Labill.) R.Br. (Olacaceaea) and its multiple hosts. Plant, Cell & Environment 17, 1263–1273.
| Crossref | GoogleScholarGoogle Scholar |
Peterlunger K,
Marangoni B, Testolin R
(1990) Carbohydrates, organic acids and mineral elements in xylem sap bleeding from kiwifruit canes. Acta Horticulturae 282, 273–282.
Pires CSS,
Price PW,
Sujii ER, Avelar C
(2000) Feeding behaviour of the spittlebug Deois flavopicta (Homoptera: Cercopidae) on wild and cultivated host plants. Environmental Entomology 29, 750–757.
Ponder KL,
Watson RJ,
Malone M, Pritchard J
(2002) Mineral content of excreta from the spittlebug Philaenus spumarius closely matches that of xylem sap. New Phytologist 153, 237–242.
| Crossref | GoogleScholarGoogle Scholar |
Rossi AM,
Brodbeck BV, Strong DR
(1996) Response of xylem-feeding leafhopper to host plant species and plant quality. Journal of Chemical Ecology 22, 653–671.
| Crossref | GoogleScholarGoogle Scholar |
Schurr U
(1998) Xylem sap sampling – new approaches to an old topic. Trends in Plant Science 3, 293–298.
| Crossref | GoogleScholarGoogle Scholar |
Siebrecht S,
Herdel K,
Schurr U, Tischner R
(2003) Nutrient translocation in the xylem of poplar-diurnal variations and spatial distribution along the shoot axis. Planta 217, 783–793.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Smith GS,
Gravett IM,
Edwards CM,
Curtis JP, Buwalda JG
(1994) Spatial analysis of the canopy of kiwifruit vines as it relates to the physical, chemical and post-harvest attributes of the fruit. Annals of Botany 73, 99–111.
| Crossref | GoogleScholarGoogle Scholar |
Sotiropoulos TE,
Therios IN, Dimassi KN
(2002) Seasonal variation and chemical composition of bleeding xylem sap of kiwifruit vines irrigated with high boron water. Journal of Plant Nutrition 25, 1239–1248.
| Crossref | GoogleScholarGoogle Scholar |
Thompson V
(1994) Spittlebug indicators of nitrogen-fixing plants. Ecological Entomology 19, 391–398.
Thorp TG,
Ferguson IB,
Boyd LM, Barnett AM
(2003a) Fruiting position, mineral concentration and incidence of physiological pitting in ‘Hayward’ kiwifruit. Journal of Horticultural Science & Biotechnology 78, 505–511.
Thorp TG,
Barnett AM, Miller SA
(2003b) Effects of cane size and pruning system on shoot growth, flowering and productivity of ‘Hayward’ kiwifruit vines. Journal of Horticultural Science & Biotechnology 78, 219–224.
Turner NA,
Ferguson IB, Sharples RO
(1977) Sampling and analysis for determining relationship of calcium concentration to bitter pit in apple fruit. New Zealand Journal of Agricultural Research 20, 525–532.
Tyree MT,
Graham MED,
Cooper KE, Bazos LJ
(1983) The hydraulic architecture of Thuja occidentalis. Canadian Journal of Botany 61, 2105–2111.
Watson RJ,
Pritchard J, Malone M
(2001) Direct measurement of sodium and potassium in the transpiration stream of salt-excluding and non-excluding varieties of wheat. Journal of Experimental Botany 52, 1873–1881.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Xiloyannis C,
Celano G,
Sebastiani L, Minnocci A
(2001) Water relations, calcium and potassium concentration in fruits and leaves during annual growth in mature kiwifruit plants. Acta Horticulturae 564, 129–134.