Abstract
Key message
In this review, the main internal and environmental hypotheses regarding alternate bearing and abscission of inflorescence buds and also, the methods to mitigate this physiological phenomenon have been investigated.
Abstract
Alternate bearing is annually fluctuating heavy (‘on’) and light (‘off’) crops, which occurs in most fruit trees. There are multiple visible causes, decreased shoot growth and flower buds or imperfect flowers, but all occur in association with a heavy crop, suggesting a carbohydrate resource limitation to shoot growth, or flower initiation, induction or differentiation. Pistachios bear on 1-year-old shoots from axillary buds produced the previous year. The visible mechanism is bud abscission on current season’s growth during ‘on’ years and bud retention in low crop load (‘off’) years. Though bud abscission is visible, the underlying cause is unknown. This review classifies the multiple hypotheses as internal, genetic, carbohydrate resources and hormones or environmental, abiotic and biotic stresses. Our examination of potential hypotheses and recent research suggests alternate bearing in pistachio is a result of the carbohydrate resource limitation generated by the heavy ‘on’ year crop maturation. However, the specific signal producing bud abscission is unknown. Alternate bearing in pistachio can be mitigated by a vigorous rootstock, particularly if combined with proper pruning. We hypothesize the vigorous rootstock may produce a better carbohydrate resource status through a larger tree with more leaf surface area. The pruning does not address the bud abscission but alters the ratio of non-bearing to bearing shoots, resulting in a lower alternate bearing index. Furthermore, we conclude alternate bearing in pistachio, while a within shoot phenomenon, can be triggered by severe environmental events that damage a current crop.
Similar content being viewed by others
References
Abrishami MH (1995) Persian pistachio. A comprehensive history. University Press, Tehran (In Persian)
Addicott FT (1982) Abscission. University of California Press, Berkeley
Alam SN (1999) Nutrient uptake by plants under stress conditions. In: Pessarakli M (ed) Handbook of plant and crop stress. CRC Press Inc., Boca Raton, pp 285–313
Alcázar R, Marco F, Cuevas JC, Patron M, Ferrando A, Carrasco P, Tiburcio AF, Altabella T (2006) Involvement of polyamines in plant response to abiotic stress. Biotechnol Lett 28:1867–1876
Anagnostopoulos P (1938) Physiological disorders of pistachio. Pomol Res 3:581–592 (In Greek)
Baninasab B, Rahemi M (2006) Possible role of non-structural carbohydrate in alternate bearing of pistachio. Eur J Hort Sci 71:277–282
Baninasab B, Rahemi M (2008) Effect of exogenous polyamines on flower bud retention in pistachio (Pistacia vera L.) trees. Hortic Environ Biotechnol 49:149–154
Baninasab B, Rahemi M, Javanshah A (2007) Effects of time of foliar application of nitrogen and its concentrations on the flower bud retention in pistachio trees. Int J Soil Sci 2:40–47
Beede RH, Ferguson L (2015) Effect of hedging and topping on pistachio alternate bearing. Amer Pistachio Ind Ann Rep, Crop Year 2014–2015:94–97
Beede RH, Ferguson L, Rose D, Padilla J (1991) Effect of pruning on the yield components of pistachio. CA Pistachio Ind Ann Rep, Crop Year 1990–91:90–93
Beede RH, Brown PH, Kallsen C, Weinbaum SA (2016) Diagnosing and correcting nutrient deficiencies. In: Ferguson L, Haviland DR (Eds) Pistachio production manual. University of California, Agricultural and Natural Resources Publication No. 3545, pp 173–188
Beede RH, Ferguson L, Lampinen B, Metcaf S (2017) Effect of hedging and topping on pistachio alternate bearing: 2012–2017. Amer Pistachio Ind Ann Rep Crop Year 2017–2018
Bentley WJ, Goodell PB, Beede RH (2016) Small bugs: neurocolpus, phytocoris, calocoris, and lygus. In: Ferguson L, Haviland DR (eds) Pistachio production manual. University of California, Agricultural and Natural Resources Publication. No. 3545, pp 215–224
Bita CE, Gerats T (2013) Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci 4:1–18
Boss PK, Bastow RM, Mylne JS, Dean C (2004) Multiple pathways in the decision to flower: enabling, promoting, and resetting. Plant Cell 16:18–31
Brown PH, Weinbaum SA, Picchioni GA (1995) Alternate bearing influences annual nutrient consumption and the total nutrient content of mature pistachio trees. Trees 9:158–164
Chadzinikolaou AN (1951) The pistachio. Ministry of Agriculture Directorate of Agricultural Studies and Research, Athens (In Greek)
Corbesier L, Vincent C, Jang S, Fornara F, Fan Q, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C, Coupland G (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Sci 316:1030–1033
Crane JC, Al-Shalan I (1977) Carbohydrate and nitrogen levels in pistachio branches as related to shoot extension and yield. J Am Soc Hortic Sci 102:326–399
Crane JC, Iwakiri BT (1981) Morphology and reproduction of pistachio. Hortic Rev 3:376–393
Crane JC, Iwakiri BT (1985) Vegetative and reproductive dominance in pistachio. HortScience 20:1092–1093
Crane JC, Iwakiri BT (1986) Pistachio yield and quality as affected by rootstock. HortScience 21:1139–1140
Crane JC, Iwakiri BT (1987) Reconsideration of the cause of inflorescence bud abscission in pistachio. HortScience 22:1315–1316
Crane JC, Nelson MM (1971) The unusual mechanism of alternate bearing in the pistachio. HortScience 6:489–490
Crane JC, Nelson MM (1972) Effects of crop load, girdling and auxin application on alternate bearing of the pistachio. J Am Soc Hortic Sci 97:337–339
Crane JC, Al-Shalan I, Carlson RM (1973) Abscission of pistachio inflorescence buds as affected by leaf area and number of nuts. J Am Soc Hortic Sci 98:591–592
Crane JC, Catlin PB, Al-Shalan I (1976) Carbohydrate levels in the pistachio as related to alternate bearing. J Am Soc Hortic Sci 101:371–374
Crane JC, Iwakiri BT, Lin TS (1982) Effects of ethephon on shell dehiscence and flower bud abscission in pistachio. HortScience 17:383–384
Daane KM, Yokota GY, Krunger R, Steffan SA, da Silva PG, Beede RH, Bentley WJ, Weinberger GB (2005) Large bugs damage pistachio nuts most severely during midseason. Calif Agric 59:95–102
Davis LD (1957) Flowering and alternate bearing. J Am Soc Hortic Sci 70:545–556
Doster WA, Michailides TJ (1995) The relationship between date of hull splitting and decay of pistachio nuts by Aspergillus species. Plant Dis 79:766–769
Durzan DJ (1996) Nitrogen reallocation during female bud abscission in alternate bearing of pistachio. Adv Hortic Sci 10:219–225
Esmailpour A (2005) Evaluation of alternate bearing intensity in Iranian pistachio cultivars. Options Méditerranéennes Ser A 63:29–32
Esmailpour A, Khezri M (2006) Abscission of inflorescence buds as affected by genetic characteristics in some Iranian commercial pistachio cultivars. Int J Agric Biol 8:360–362
FAO (2017) FAOSTAT database collections. Food and Agriculture Organization of the United Nations. Rome. https://faostat.fao.org. Accessed 19 Dec 2018
Ferguson L (1985) Effect of foliar urea applications on leaf nitrogen content and bud retention in pistachio. CA Pistachio Ind Annu Rep 94–95
Ferguson L (1986) Effects of growth regulators on shoot extension, bud differentiation and bud retention of pistachios. CA Pistachio Ind Ann Rep Crop, Year 1985–1986(92):93
Ferguson L, Kallsen CE (2016) The pistachio tree: physiology and botany. In: Ferguson L, Haviland DR (eds) Pistachio production manual. University of California, Agricultural and Natural Resources Publication. No. 3545, pp 17–19
Ferguson L, Maranto J (1989) Effect of growth regulators on pistachio inflorescence bud retention. Calif Pistachio Ind Annu Rep Crop Year 1988–1989:91–92
Ferguson L, Polito VS (2016) Alternate bearing, nut blanking and shell splitting. In: Ferguson L, Haviland DR (eds) Pistachio production manual. University of California, Agricultural and Natural Resources Publication. No. 3545, pp 313–314
Ferguson L, Maranto J, Beede RH (1995) Mechanical topping mitigates alternate bearing of ‘Kerman’ pistachios (Pistacia vera L.). HortScience 30:1369–1375
Ferguson L, Beede RH, Haviland DR, Beyes H, Sanden BL, Grattan, SR, Epstein L (2016) Pistachio rootstocks. In: Ferguson L, Haviland DR (eds) Pistachio production manual. University of California, Agricultural and Natural Resources Publication. No. 3545, pp 65–74
Gawad H, Ferguson L (1987) Effect of growth regulators on pistachio inflorescence bud retention: a preliminary report. Calif Pistachio Comm Annu Rep Crop Year 1986–1987:78–81
Goldschmidt EE (2013) The evolution of fruit tree productivity: a review. Econ Bot 67:51–62
Goldhamer DA, Snyder RL (1989) Irrigation scheduling: a guide for efficient on-farm water management, Division of Agriculture and Natural Resources, University of California, Oakland. Publication 21454
Goldhamer DA, Kjelgren RK, Williams L, Beede R (1985) Water use requirements of pistachio trees and response to water stress. In: Proceedings of the national conference on advances in evapotranspiration. American Society of Agricultural Engineers, pp 216–223
Glodhamer DA, Kanber R (2012) Pistachio. In: Crop yield response to water. FAO Irrigation and Drainage Paper No. 66. Food and Agriculture Organization of the United Nations, Rome, Italy, pp 416–429
Guitton B, Kelner JJ, Velasco R, Gardiner SE, Chagne D, Costes E (2012) Genetic control of biennial bearing in apple. J Exp Bot 63:131–149
Gunes NT, Okay Y, Koksal AI, Koroglu M (2010) The effect of nitrogen and phosphorus fertilization on yield, some fruit characteristics, hormone concentrations, and alternate bearing in pistachio. Turk J Agric For 34:33–43
Hasanuzzaman M, Nahar K, Alam MM, Roychowdhury R, Masayuki F (2013) Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci 14:9643–9684
Haviland D, Beede RH, Daane K (2008) Mealybugs. Pistachio Production Manual, 5th edn. Fruit and Nut Research and Information, Center University of California, Davis, pp 220–222
Heerema RJ, Weinbaum SA, Pernice F, DeJong TM (2008) Spur survival and return bloom in almond [Prunus dulcis (Mill.) DA Webb] varied with spur fruit load, specific leaf weight, and leaf area. J Hortic Sci Biotechnol 83:274–281
Herrera E (1997) Growing pistachios in New Mexico. Cooperative Extension Service. No. 532, p 13
Hoblyn T, Grubb A, Painter A, Wates B (1936) Studies in biennial bearing. I J Pomol Hortic Sci 14:39–76
Hokmabadi H (2010) Pistachio frost damage in Iran and new methods of frost protection. Options Méditerranéennes 94:71–78
Hormaza JI, Polito VS (1996) Pistillate and staminate flower development in dioecious Pistacia vera (pistachio, Anacardiaceae). Am J Bot 83:759–766
Hormaza JI, Wünsch A (2007) Pistachio. In: Kole C (ed) Genome mapping and molecular breeding in plants. Fruits and nuts, Germany, pp 243–252
IPGRI (1997) Descriptors for pistachio (Pistacia vera L.). International plant genetic resources, Rome
Johnson RS, Weinbaum SA (1987) Variation in tree size, yield, cropping efficiency, and alternate bearing among Kerman Pistachio trees. J Am Soc Hortic Sci 112:942–945
Kallsen CE (2007) Pistachio notes. University of California Cooperative Extension, Santa Rosa
Kallsen CE, Parfitt DE, Holtz BA (2007) Early differences in the intensity of alternate bearing among selected pistachio genotypes. HortScience 42:1740–1743
Kallsen CE, Parfitt DE, Maranto J, Holtz BA (2009) New pistachio varieties show promise for California cultivation. Calif Agric 63:18–23
Kallsen CE, Parfitt DE, Holtz BA (2014) Comparison of bloom and harvest dates, alternate bearing index and nut quality parameters of ‘Golden Hills’ and ‘Lost Hills’ pistachio cultivars to ‘Kerman’. Acta Hortic 1028:279–283
Khezri M (2010) Effect of rootstocks and spray application of nitrogen, boron, zinc and free polyamines on some physiological problems and yield of pistachio (Pistacia vera cv. Kaleh-Ghoochi). Ph.D dissertation. University of Tehran, Iran (In Persian)
Khezri M (2013) Study of time intervals of inflorescence bud abscission and some morphological and physiological traits of ‘on’ and ‘off’ pistachio trees. SBUK Final Report. University of Kerman, Iran, No. 716/41 (In Persian)
Khezri M, Talaie A, Javanshah A, Hadavi F (2010) Effect of exogenous application of free polyamines on physiological disorders and yield of ‘Kaleh-Ghoochi’ pistachio shoots (Pistacia vera L.). Sci Hortic 125:270–276
Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T (1999) A pair of related genes with antagonistic roles in mediating flowering signals. Science 286:1960–1962
Lin TS, Crane JC, Polito VS (1984a) Anatomical aspects of abscission in pistachio. J Am Soc Hortic Sci 109:69–73
Lin TS, Crane JC, Ryugo K (1984b) Gibberellin-like substances in pistachio as related to inflorescence bud abscission. HortScience 19:267–268
Lovatt CJ, Ferguson L (1994) Using foliar application of urea combined with 6-benzyladenine to decrease pistachio floral bud abscission in an on-year to increase yield the next year. CA Pistachio Ind Ann Rep 155–158
Lovatt CJ, Daoudi H, Ferguson L (2005) Efficacy of foliar-applied cytokinins and nitrogen to increase floral bud retention and to reduce alternate bearing of pistachio. Acta Hortic 727:353–364
Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158
Marino G, La Mantia M, Caruso T, Marra FP (2018) Seasonal dynamics of photosynthesis and total carbon gain in bearing and nonbearing pistachio (Pistacia vera L.) shoots. Photosynthetica 56:932–941
Martinelli F, Marchese A, Balan B, Giovino A, Caruso T, Fretto S, Marra FP (2018) RNA-Seq analysis to investigate alternate bearing mechanism in Pistacia vera L. Acta Hortic 1229:71–78
Mehrnejad M (2001) The current status of pistachio pests in Iran. Cahiers Options Méditerranéennes 56:315–322
Michailides TJ (1990) Three common pests of pistachio in California. Calif Agric 44:6–8
Michailides TJ, Morgan DP, Doster MA (1995) Diseases of pistachio in California and their significance. Acta Hortic 419:337–343
Monselise SP, Goldschmidt EE (1982) Alternate bearing in fruit trees. Hortic Rev 4:128–173
Muñoz-Fambuena N, Mesejo C, González-Mas MC, Primo-Millo E, Agustí M, Iglesias DJ (2012) Fruit load modulates flowering-related gene expression in buds of alternate-bearing 'Moncada' mandarin. Ann Bot 110:1109–1118
Nzima MDS, Martin GC, Nishijima C (1997a) Seasonal changes in total nonstructural carbohydrates within branches and roots of naturally "off" and "on" 'Kerman' pistachio trees. J Am Soc Hortic Sci 122:856–862
Nzima MDS, Martin GC, Nishijima C (1997b) Leaf development, dry matter accumulation, and distribution within branches of alternate-bearing 'Kerman' pistachio trees. J Am Soc Hortic Sci 122:31–37
Nzima MDS, Martin GC, Nishijima C (1999) Effects of fall defoliation and spring shading on shoot carbohydrate and growth parameters among individual branches of alternate bearing ‘Kerman’ pistachio trees. J Am Soc Hortic Sci 124:52–60
Pakkish Z, Rahemi M, Panahi B (2011) Low temperature resistance of developing flower buds of pistachio. J Biol Environ Sci 5:153–157
Panahi B, Khezri M (2011) Effect of harvesting time on nut quality of pistachio (Pistacia vera L.) cultivars. Sci Hortic 256:110–120
Parfitt DE, Kafkas S, Batle I, Vargas FJ, Kallsen CE (2012) Pistachio. In: Badenes ML, Byrne DH (eds) Fruit breeding. Springer, New York, p 875
Pearce SC, Dobersek-Urbanc S (1967) The measurement of irregularity in growth and cropping. J Hortic Sci 42:295–305
Pearson TC, Slaughter D, Studer HE (1996) Hull adhesion characteristics of early-split and normal pistachio nuts. Appl Eng Agric 12:219–221
Picchioni GA, Brown PH, Weinbaum SA, Muraoka TT (1997) Macronutrient allocation to leaves and fruit of mature, alternate-bearing pistachio trees: magnitude and seasonal patterns at the whole-canopy level. J Am Soc Hortic Sci 122:267–274
Pontikis CA (1990) Effects of 2-naphthaleneacetic acid on alternate bearing of pistachio. Fruits 5:281–285
Porlingis IC (1974) Flower bud abscission in pistachio as related to fruit development and other factors. J Am Soc Hortic Sci 99:121–125
Rahemi M, Ramezanian A (2007) Potential of ethephon, NAA, NAD and urea for thinning pistachio fruitlets. Sci Hortic 111:160–163
Reid MS (1985) Ethylene and abscission. HortScience 20:45–50
Rosecrance RC, Weinbaum SA, Brown PH (1996) Assessment of nitrogen, phosphorus, and potassium uptake capacity and root growth in mature alternate-bearing pistachio (Pistacia vera) trees. Tree Physiol 16:949–956
Rosecrance RC, Weinbaum SA, Brown PH (1998) Alternate bearing affects nitrogen, phosphorus, potassium and starch storage pools in mature pistachio trees. Ann Bot 82:463–470
Rosenstock T, Rosa UA, Plant RE, Brown PH (2010) A reevaluation of alternate bearing in pistachio. Sci Hortic 124:149–152
Roussos PA, Pontikis CA, Zoti MA (2004) The role of free polyamines in the alternate-bearing of pistachio (Pistacia vera cv. Pontikis). Trees 18:61–69
Shanker AK, Maheswari M, Yadav SK, Desai S, Bhanu D, Attal NB, Venkateswarlu B (2014) Drought stress responses in crops. Funct Integr Genomics 14:11–22
Spann TM, Beede RH, DeJong TM (2008) Seasonal carbohydrate storage and mobilization in bearing and non-bearing pistachio (Pistacia vera) trees. Tree Physiol 28:207–213
Sprugel DG, Hinckley TM, Schaap W (1991) The theory and practice of branch autonomy. Annu Rev Ecol Syst 22:309–334
Stevenson MT, Shackel KA (1998) Alternate bearing in pistachio as a masting phenomenon: construction cost of reproduction versus vegetative growth and storage. J Am Soc Hortic Sci 123:1069–1075
Stevenson MT, Shackel KA, Ferguson L (2000) Shoot length distribution and its relation to yield of alternate-bearing pistachio trees. J Am Soc Hortic Sci 125:165–168
Takeda F, Crane JC (1980) Abscisic acid in pistachio as related to inflorescence bud abscission. J Amer Soc Hort Sci 105:573–576
Takeda F, Ryugo K, Crane JC (1980) Translocation and distribution of 14C-photosynthates in bearing and nonbearing pistachio branches. J Am Soc Hortic Sci 105:642–644
Talaie A, Seyedi M, Panahi B, Khezri M (2006) Effects of shoot girdling and urea combined with 6-benzyl adenine on abscission of inflorescence buds in “Ohadi” pistachio cultivar (Pistacia vera L.). Int J Agric Biol 8:474–476
Talaie A, Lesani H, Esmaeilizadeh M, Dashti H (2010) Effect of girdling, crop Load, zinc sulfate and carbohydrate foliar application on inflorescence bud abscission and nut quality of ‘Ohadi’ pistachio. Acta Hortic 940:97–104
Tan F, Swain SM (2006) Genetics of flower initiation and development in annual and perennial plants. Physiol Plant 128:8–17
Tezerji ZS (2011) Determination of damages of pistachio twig borer moth Kermania pistaciella amsel, to fruit clusters of pistachio trees. Acta Hortic 912:701–708
Uiu K, Crane JC (1977) Mineral element changes in pistachio leaves. J Am Soc Hortic Sci 102:155–158
Vemmos SN (1994) Net photosynthesis, stomatal conductance, chlorophyll content and specific leaf weight of pistachio trees (c.v. Aegenes) as influenced by fruiting. J Hortic Sci 69:775–782
Vemmos SN (1999a) Mineral composition of leaves and inflorescent buds in fruiting and non-fruiting pistachio trees. J Plant Nutr 22:1291–1301
Vemmos SN (1999b) Carbohydrate content of inflorescent buds of defruited and fruiting pistachio (Pistacia vera L.) branches in relation to biennial bearing. J Hortic Sci Biotechnol 74:94–100
Vemmos SN (2010) Alternate bearing and the possible role of carbohydrates in bud abscission of pistachio (Pistacia vera L.). Options Méditerranéennes 94:9–18
Vemmos SN, Pontikis CA, Tolia-Marioli AP (1994) Respiration rate and ethylene production in inflorescence buds of pistachio in relation to alternate bearing. Sci Hortic 57:165–172
Vemmos SN, Papagiannopoulou A, Coward S (2012) Effects of shoot girdling on photosynthetic capacity, leaf carbohydrate, and bud abscission in pistachio (Pistacia vera L.). Photosynthetica 50:35–48
Wannan BS, Quinn CJ (1991) Floral structure and eveloution in the Anacardiaceae. Bot J Linn Soc 107:349–385
Weinbaum SA, Picchioni GA, Muraoka TT, Ferguson L, Brown PH (1994) Fertilizer nitrogen and boron uptake, storage and allocation vary during the alternate bearing cycle in pistachio trees. J Am Soc Hortic Sci 119:24–31
Wolpert JA, Ferguson L (1990) Inflorescence bud retention in ‘Kerman’ pistachios: Effects of defruiting date and branch size. HortScience 25:919–921
Wood BW (1991) Alternate bearing of pecan. In: Wood BW, Payne JA (ed) Proc. First National Pecan Workshop. U.S. Dep Agriculture-Agr. Res. Serv., ARS-96
Yanofsky MF (1995) Floral meristems to floral organs: genes controlling early events in Arabidopsis flower development. Annu Rev Plant Physiol Plant Mol Biol 46:167–188
Yoo SJ, Chung KS, Jung SH, Yoo SY, Lee JS, Ahn JH (2010) Bother of FT and TFL1 (BFT) has TFL1-like activity and functions redundantly with TFL1 in inflorescence meristem development in Arabidopsis. Plant J 63:241–253
Zhang JL (2014) A preliminary report on mechanical pruning utilizing a ‘1-side mechanical slant topping’ technique on pistachio trees. Acta Hortic 1028:351–358
Zhang JL, Shi H (2013) Physiological and molecular mechanisms of plant salt tolerance. Photosyn Res 115:1–22
Zhang Y, Zhang R (2009) Effects of ABA content on the development of abscission zone and berry falling after harvesting of grapes. Agric Sci China 8:59–67
Zwieniecki M, Sperling O (2015) Development of physiology based methods for sustainable management of pistachios under changing central valley climatic conditions. CPRB Ann Rep 19
Author information
Authors and Affiliations
Contributions
MK and RH conceived the presented idea and designed the contents of manuscript. MK collected the data and information through literatures and drafted the manuscript. RH, GB and LF approved the concepts and design of manuscript. They critically revised the manuscript several times and provided new information, interpretation and references. MK added high quality photos, made all revisions, shared the revisions with all authors and finalized the manuscript. MK, RH, GB, LF approved the final version to be published in Trees.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Marcos Buckeridge.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Khezri, M., Heerema, R., Brar, G. et al. Alternate bearing in pistachio (Pistacia vera L.): a review. Trees 34, 855–868 (2020). https://doi.org/10.1007/s00468-020-01967-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00468-020-01967-y