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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Fruit presence negatively affects photosynthesis by reducing leaf nitrogen in almond

Sebastian Saa A C and Patrick H. Brown B
+ Author Affiliations
- Author Affiliations

A Facultad de Agronomía, Pontificia Universidad Católica de Valparaíso, Casilla 4D, Quillota, Chile.

B Department of Plant Sciences, University of California, One Shields Avenue, Davis, CA 95616, USA.

C Corresponding author. Email: sebastian.saa@ucv.cl

Functional Plant Biology 41(8) 884-891 https://doi.org/10.1071/FP13343
Submitted: 28 November 2013  Accepted: 19 February 2014   Published: 1 April 2014

Abstract

Fruit presence often positively and seldom negatively affects leaf carbon assimilation rate in fruit-trees. In almond (Prunus dulcis (Mill.) DA Webb) the presence of fruit often results in the death of the fruit bearing spurs. The mechanism of this effect is unclear, but may be a consequence of diminished carbon assimilation rate in leaves adjacent to fruit and the subsequent depletion of nutrient and carbohydrates reserves. This study evaluated the influence of fruit on leaf carbon assimilation rate and leaf nitrogen throughout the season. Carbon assimilation rate (Aa), rubisco carboxylation capacity at leaf temperature (Vcmax@Tleaf), maximum rate of RubP regeneration at leaf temperature (Jmax@Tleaf), leaf nitrogen on a mass basis (N%) and area basis (Na), and specific leaf weight data were recorded. Fruit presence negatively affected leaf nitrogen concentration by a reduction in specific leaf weight and leaf nitrogen content. The impact of fruit presence on carbon assimilation rate was predominantly associated with the negative effect of fruit on Na and resulted in a significant reduction in Jmax@Tleaf and therefore in Aa, especially after full leaf and fruit expansion. The reduction in leaf area, leaf nitrogen, reduced Jmax@Tleaf and decreased carbon assimilation rate in the presence of fruit explains the negative effects of fruit presence on spur vitality.

Additional keywords: fruit and leaf competition, nitrogen competition, photosynthesis, specific leaf area, spur mortality, survival.


References

Cheng JS, Fan PG, Liang ZC, Wang YQ, Niu N, Li WD, Li SH (2009) Accumulation of end products in source leaves affects photosynthetic rate in peach via alteration of stomatal conductance and photosynthetic efficiency. Journal of the American Society for Horticultural Science 134, 667–676.

Crews CE, Williams SL, Vines HM (1975) Characteristics of photosynthesis in peach leaves. Planta 126, 97–104.
Characteristics of photosynthesis in peach leaves.Crossref | GoogleScholarGoogle Scholar | 24430151PubMed |

DeJong TM (1986) Fruit effects on photosynthesis in Prunus persica. Physiologia Plantarum 66, 149–153.
Fruit effects on photosynthesis in Prunus persica.Crossref | GoogleScholarGoogle Scholar |

Duan W, Fan PG, Wang LJ, Li WD, Yan ST, Li SH (2008) Photosynthetic response to low sink demand after fruit removal in relation to photoinhibition and photoprotection in peach trees. Tree Physiology 28, 123–132.
Photosynthetic response to low sink demand after fruit removal in relation to photoinhibition and photoprotection in peach trees.Crossref | GoogleScholarGoogle Scholar | 17938121PubMed |

Egea G, Gonzalez-Real MM, Baille A, Nortes PA, Diaz-Espejo A (2011) Disentangling the contributions of ontogeny and water stress to photosynthetic limitations in almond trees. Plant, Cell & Environment 34, 962–979.
Disentangling the contributions of ontogeny and water stress to photosynthetic limitations in almond trees.Crossref | GoogleScholarGoogle Scholar |

Egea G, Gonzalez-Real MM, Baille A, Nortes PA, Conesa MR, Ruiz-Salleres I (2012) Effects of water stress on irradiance acclimation of leaf traits in almond trees. Tree Physiology 32, 450–463.
Effects of water stress on irradiance acclimation of leaf traits in almond trees.Crossref | GoogleScholarGoogle Scholar | 22440881PubMed |

Ethier GJ, Livingston NJ (2004) On the need to incorporate sensitivity to CO2 transfer conductance into the Farquhar-von Caemmerer-Berry leaf photosynthesis model. Plant, Cell & Environment 27, 137–153.
On the need to incorporate sensitivity to CO2 transfer conductance into the Farquhar-von Caemmerer-Berry leaf photosynthesis model.Crossref | GoogleScholarGoogle Scholar |

Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78, 9–19.
Photosynthesis and nitrogen relationships in leaves of C3 plants.Crossref | GoogleScholarGoogle Scholar |

Evans JR, Poorter H (2001) Photosynthetic acclimation of plants to growth irradiance: the relative importance of specific leaf area and nitrogen partitioning in maximizing carbon gain. Plant, Cell & Environment 24, 755–767.
Photosynthetic acclimation of plants to growth irradiance: the relative importance of specific leaf area and nitrogen partitioning in maximizing carbon gain.Crossref | GoogleScholarGoogle Scholar |

Fan PG, Li LS, Duan W, Li WD, Li SH (2010) Photosynthesis of young apple trees in response to low sink demand under different air temperatures. Tree Physiology 30, 313–325.
Photosynthesis of young apple trees in response to low sink demand under different air temperatures.Crossref | GoogleScholarGoogle Scholar | 20071359PubMed |

Farquhar GD, Caemmerer SV, Berry JA (1980) A biochemical-model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78–90.
A biochemical-model of photosynthetic CO2 assimilation in leaves of C3 species.Crossref | GoogleScholarGoogle Scholar | 24306196PubMed |

Field C, Mooney HA (1986) The photosynthesis-nitrogen relationship in wild plants. In ‘On the economy of plant form and function’. (Ed. TH Givnish) pp. 25–56. (Cambridge University Press: Cambridge)

Fujii JA, Kennedy RA (1985) Seasonal-changes in the photosynthetic rate in apple trees: a comparison between fruiting and non fruiting trees. Plant Physiology 78, 519–524.
Seasonal-changes in the photosynthetic rate in apple trees: a comparison between fruiting and non fruiting trees.Crossref | GoogleScholarGoogle Scholar | 16664276PubMed |

Hansen P (1969) 14C-studies on apple trees. Photosynthate consumption in fruits in relation to leaf-fruit ratio and to leaf-fruit position. Physiologia Plantarum 22, 186–198.
14C-studies on apple trees. Photosynthate consumption in fruits in relation to leaf-fruit ratio and to leaf-fruit position.Crossref | GoogleScholarGoogle Scholar |

Hansen P (1971) Effect of fruiting upon transpirtation rate and stomatal opening in apple leaves. Physiologia Plantarum 25, 181–183.
Effect of fruiting upon transpirtation rate and stomatal opening in apple leaves.Crossref | GoogleScholarGoogle Scholar |

Heerema RJ, Weinbaum SA, Pernice F, Dejong TM (2008) Spur survival and return bloom in almond Prunus dulcis (Mill.) DAWebb varied with spur fruit load, specific leaf weight, and leaf area. Journal of Horticultural Science & Biotechnology 83, 274–281.

Heerema RJ, Weinbaum SA, Lampinen BD, Dejong TM (2009) Is nitrogen stress more apparent in shaded, fruiting almond spurs than in exposed, non-fruiting spurs? Journal of Horticultural Science & Biotechnology 84, 355–359.

Kester DE, Martin GC, Labavitch JM (1996) Growth and Development. In ‘Almond production manual’. pp. 90–97. (University of California Division of Agricultural and Natural Resources: Oakland, CA, USA)

Lampinen BD, Tombesi S, Metcalf SG, DeJong TM (2011) Spur behaviour in almond trees: relationships between previous year spur leaf area, fruit bearing and mortality. Tree Physiology 31, 700–706.
Spur behaviour in almond trees: relationships between previous year spur leaf area, fruit bearing and mortality.Crossref | GoogleScholarGoogle Scholar | 21849590PubMed |

McCutchan H, Shackel KA (1992) Stem water potential as a sensitive indicator of water stress in prune trees (Prunus domestica L. cv. Fench). Journal of the American Society for Horticultural Science 117, 607–611.

Micke W (1996) ‘Almond production manual.’ (University of California Division of Agricultural and Natural Resources: Oakland, CA, USA)

Niinemets U (1997) Role of foliar nitrogen in light harvesting and shade tolerance of four temperate deciduous woody species. Functional Ecology 11, 518–531.
Role of foliar nitrogen in light harvesting and shade tolerance of four temperate deciduous woody species.Crossref | GoogleScholarGoogle Scholar |

Niinemets U, Tenhunen JD (1997) A model separating leaf structural and physiological effects on carbon gain along light gradients for the shade-tolerant species Acer saccharum. Plant, Cell & Environment 20, 845–866.
A model separating leaf structural and physiological effects on carbon gain along light gradients for the shade-tolerant species Acer saccharum.Crossref | GoogleScholarGoogle Scholar |

Nortes PA, Gonzalez-Real MM, Egea G, Baille A (2009) Seasonal effects of deficit irrigation on leaf photosynthetic traits of fruiting and non-fruiting shoots in almond trees. Tree Physiology 29, 375–388.
Seasonal effects of deficit irrigation on leaf photosynthetic traits of fruiting and non-fruiting shoots in almond trees.Crossref | GoogleScholarGoogle Scholar | 19203958PubMed |

Palmer JW, Giuliani R, Adams HM (1997) Effect of crop load on fruiting and leaf photosynthesis of ‘Braeburn’/M.26 apple trees. Tree Physiology 17, 741–746.
Effect of crop load on fruiting and leaf photosynthesis of ‘Braeburn’/M.26 apple trees.Crossref | GoogleScholarGoogle Scholar | 14759899PubMed |

Reidel EJ, Brown PH, Duncan RA, Heerema RJ, Weinbaum SA (2004) Sensitivity of yield determinants to potassium deficiency in ‘Nonpareil’ almond (Prunus dulcis (Mill.) DA Webb). Journal of Horticultural Science & Biotechnology 79, 906–910.

Ripullone F, Grassi G, Lauteri M, Borghetti M (2003) Photosynthesis-nitrogen relationships: Interpretation of different patterns between Pseudotsuga menziesii and Populus × euroamericana in a mini-stand experiment. Tree Physiology 23, 137–144.
Photosynthesis-nitrogen relationships: Interpretation of different patterns between Pseudotsuga menziesii and Populus × euroamericana in a mini-stand experiment.Crossref | GoogleScholarGoogle Scholar | 12533308PubMed |

Samach A, Smith HM (2013) Constraints to obtaining consistent annual yields in perennials. II: Environment and fruit load affect induction of flowering. Plant Science 207, 168–176.
Constraints to obtaining consistent annual yields in perennials. II: Environment and fruit load affect induction of flowering.Crossref | GoogleScholarGoogle Scholar | 23602112PubMed |

Sams CE, Flore JA (1983) Net photosynthetic rate of sour cherry (Prunus cerasus L. ‘Montmorency’) during the growing-season with particular reference to fruiting. Photosynthesis Research 4, 307–316.
Net photosynthetic rate of sour cherry (Prunus cerasus L. ‘Montmorency’) during the growing-season with particular reference to fruiting.Crossref | GoogleScholarGoogle Scholar | 24458524PubMed |

Sharkey TD, Bernacchi CJ, Farquhar GD, Singsaas EL (2007) Fitting photosynthetic carbon dioxide response curves for C3 leaves. Plant, Cell & Environment 30, 1035–1040.
Fitting photosynthetic carbon dioxide response curves for C3 leaves.Crossref | GoogleScholarGoogle Scholar |

Silber A, Israeli Y, Levi M, Keinan A, Chudi G, Golan A, Noy M, Levkovitch I, Narkis K, Naor A, Assouline S (2013) The roles of fruit sink in the regulation of gas exchange and water uptake: a case study for avocado. Agricultural Water Management 116, 21–28.
The roles of fruit sink in the regulation of gas exchange and water uptake: a case study for avocado.Crossref | GoogleScholarGoogle Scholar |

Smith HM, Samach A (2013) Constraints to obtaining consistent annual yields in perennial tree crops. I: Heavy fruit load dominates over vegetative growth. Plant Science 207, 158–167.
Constraints to obtaining consistent annual yields in perennial tree crops. I: Heavy fruit load dominates over vegetative growth.Crossref | GoogleScholarGoogle Scholar | 23602111PubMed |

Syvertsen JP, Goni C, Otero A (2003) Fruit load and canopy shading affect leaf characteristics and net gas exchange of ‘Spring’ navel orange trees. Tree Physiology 23, 899–906.
Fruit load and canopy shading affect leaf characteristics and net gas exchange of ‘Spring’ navel orange trees.Crossref | GoogleScholarGoogle Scholar | 14532013PubMed |

Tombesi S, Lampinen BD, Metcalf S, DeJong TM (2011) Relationships between spur- and orchard-level fruit bearing in almond (Prunus dulcis). Tree Physiology 31, 1413–1421.
Relationships between spur- and orchard-level fruit bearing in almond (Prunus dulcis).Crossref | GoogleScholarGoogle Scholar | 22158011PubMed |

Turgeon R (2006) Phloem loading: how leaves gain their independence. Bioscience 56, 15–24.
Phloem loading: how leaves gain their independence.Crossref | GoogleScholarGoogle Scholar |

Urban L, Lechaudel M (2005) Effect of leaf-to-fruit ratio on leaf nitrogen content and net photosynthesis in girdled branches of Mangifera indica L. Trees – Structure and Function 19, 564–571.
Effect of leaf-to-fruit ratio on leaf nitrogen content and net photosynthesis in girdled branches of Mangifera indica L.Crossref | GoogleScholarGoogle Scholar |

Walcroft A, Le Roux X, Diaz-Espejo A, Dones N, Sinoquet H (2002) Effects of crown development on leaf irradiance, leaf morphology and photosynthetic capacity in a peach tree. Tree Physiology 22, 929–938.
Effects of crown development on leaf irradiance, leaf morphology and photosynthetic capacity in a peach tree.Crossref | GoogleScholarGoogle Scholar | 12204849PubMed |

Wu BH, Huang HQ, Fan PG, Li SH, Liu GJ (2008) Photosynthetic responses to sink-source manipulation in five peach cultivars varying in maturity date. Journal of the American Society for Horticultural Science 133, 278–283.

Wunsche JN, Palmer JW, Greer DH (2000) Effects of crop load on fruiting and gas-exchange characteristics of ‘Braeburn’/M.26 apple trees at full canopy. Journal of the American Society for Horticultural Science 125, 93–99.

Wunsche JN, Greer DH, Laing WA, Palmer JW (2005) Physiological and biochemical leaf and tree responses to crop load in apple. Tree Physiology 25, 1253–1263.
Physiological and biochemical leaf and tree responses to crop load in apple.Crossref | GoogleScholarGoogle Scholar | 16076774PubMed |

Yamori W, Nagai T, Makino A (2011) The rate-limiting step for CO2 assimilation at different temperatures is influenced by the leaf nitrogen content in several C3 crop species. Plant, Cell & Environment 34, 764–777.
The rate-limiting step for CO2 assimilation at different temperatures is influenced by the leaf nitrogen content in several C3 crop species.Crossref | GoogleScholarGoogle Scholar |

Zhang W-W, Fu X-Z, Peng L-Z, Ling L-L, Cao L, Ma X-H, Xie F, Li C (2013) Effects of sink demand and nutrient status on leaf photosynthesis of spring-cycle shoot in ‘Newhall’ navel orange under natural field conditions. Scientia Horticulturae 150, 80–85.
Effects of sink demand and nutrient status on leaf photosynthesis of spring-cycle shoot in ‘Newhall’ navel orange under natural field conditions.Crossref | GoogleScholarGoogle Scholar |