Changes in endogenous auxin level during flower bud abscission process in Pistachio (Pistacia vera L.)

The regulation of auxin (indole-3-acetic acid, IAA) level in plants is a complex mechanism and the concept is not completely understood. There are many lines of evidence suggesting that amino acid conjugates of IAA play a vital role in auxin homeostasis, but the involved plant enzymes are still under investigation. In the present study, the alteration in the levels of auxin and its conjugates in the different physiological stages and organs, as well as its role in flower bud abscission in Pistacia vera L., were investigated. The levels of the auxin and its conjugates, such as IAA, indole butyric acid (IBA), IAA-Ala, IAA-Leu, IAA-Asp, and IAA-Glu, were analyzed by ultraperformance liquid chromatography-electrospray ionization-mass spectrometry (UPLC/ESI-MS/MS) technique. Among the auxin conjugates, IAA was the main conjugate and dominant indole detected in pistachio extract observed in this work. It has also been determined that quite a few organs of 'Off-year' trees have higher auxin content than 'On-year' trees. It was observed that the auxin level is low in fruit-bearing trees in both leaves and shoots. It affects fruit yield and fruit bud abscission and plays some role in the alternate bearing. Decreased levels of auxin were observed in most of the organs of 'On-year' trees during kernel development resulting in bud abscission. This study shows that auxin conjugates play an important role in IAA metabolism, particularly in flower bud abscission and fruit kernel development.

___

  • Abel S, Theologis A (2010). Odyssey of auxin. Cold Spring Harbor Perspectives in Biology 2 (10): a004572.
  • Abrams SR, Nelson K, Ambrose SJ (2003). Deuterated abscisic acid analogs for mass spectrometry and metabolism studies. Journal of Labelled Compounds and Radiopharmaceuticals: The Official Journal of the International Isotope Society 46 (3): 273-283.
  • Acar I, Arpacı S, Bilgel L, Sürücü A, Ak BE (2011). Adaptation of some pistachio cultivars to irrigated conditions for southeast of Turkey. In: Ak BE, Wirthensohn M, Gradziel T, (editors). In: Proceedings of the 5th International Symposium on Pistachios and Almonds, 6–10 October 2009; Sanlıurfa, Turkey. Acta Horticulturae 912: 313-319.
  • Acar I, Tahtaci SA, Arpaci S, Aydin Y, Karadag S (2006). Determination of effects of plant growth regulator applications on alternate bearing in pistachios under suitable growing conditions. Acta Horticulturae 726: 539-544.
  • Ak BE, Kaşka N (1992). Antepfıstığı yetiştiriciliğinde Sık Dikimin Verime Etkisi Üzerine Bir Araştırma. Türkiye I. Ulusal Bahçe Bitkileri Kongresi. 13-16 Ekim 1992 Cilt I (Meyve), 63-66 s. (In Turkish).
  • Andersson B, Sandberg G (1982). Identification of endogenous N-(3- indolacetyl) aspartic acid in Scots pine (Pinus sylvestris L.) by combined gas chromatography–mass spectrometry, using highperformance liquid chromatography for quantification. Journal of Chromatography A 238 (1): 151-156.
  • Ayfer M (1967). The relations between megasporogenesis, embryogenesis and fruit dropping in pistachio. Ministry of Agriculture, Technical Books, D-414 (in Turkish).
  • Ayfer M, Okay Y, Erdoan V (1990). The embryo formation and development in pistachio. The First Pistachio Congress of Turkey, Proceedings, Gaziantep (in Turkish), pp. 96-106.
  • Baktir I, Ulger S, Himelrick DG (2004). Relationship of seasonal changes in endogenous plant hormones and alternate bearing of olive trees. HortScience 39 (5): 987-990.
  • Bandurski RS, Reinecke DM, Cohen JD, Slovin JP (1995). Auxin biosynthesis and metabolism. In: Davies PJ (editor). Plant Hormones: Physiology, Biochemistry and Molecular Biology. Dordrecht, the Netherlands: Kluwer Academic Press, pp. 35- 57.
  • Barlier I, Kowalczyk M, Marchant A, Ljung K, Bhalerao R et al. (2000). The SUR2 gene of Arabidopsis thaliana encodes the cytochrome P450 CYP83B1, a modulator of auxin homeostasis. Proceedings of the National Academy of Sciences 97 (26): 14819-14824.
  • Bartel B (1997). Auxin biosynthesis. Annual review of plant biology 48 (1): 51-66.
  • Bartel B, LeClere S, Magidin M, Zolman BK (2001). Inputs to the active indole-3-acetic acid pool: de novo synthesis, conjugate hydrolysis, and indole-3-butyric acid b-oxidation. Journal of Plant Growth Regulation 20 (3): 198-216.
  • Bialek K, Cohen JD (1986). Isolation and partial characterization of the major amide-linked conjugate of indole-3-acetic acid from Phaseolus vulgaris L. Plant Physiology 80 (1): 99-104.
  • Bialek K, Cohen JD (1992). Amide-linked indole acetic acid conjugates may control levels of indole acetic acid in germinating seedlings of Phaseolus vulgaris. Plant Physiology 100 (4): 2002-2007.
  • Bons HK, Kaur N, Rattanbal HS (2015). Quality and quantity improvement of citrus: role of plant growth regulators. International Journal of Agriculture, Environment and Biotechnology 8 (2): 433-447.
  • Cetinkaya H (2004). Relationship between alternate bearing and levels of hormones, carbohydrate and plant nutrients on some pistachio cultivars bearing complete or rational alternately. MSc, University of Çukurova, Institute of Natural and Applied Sciences, Adana, Turkey.
  • Cetinkaya H, Kulak M, Özgüven AI (2018). Relationship between vegetative growth and nut characteristics in alternate bearing pistachio (Pistacia vera L.) cultivars exposed to drought. The International Conference of the University of Agronomic Sciences and Veterinary Medicine of Bucharest, “Agriculture for Life, Life for Agriculture” 07–09 June 2018, Bucharest, Romania. Book of Abstracts, Section 2, Horticulture, p. 39.
  • Cetinkaya H, Özgüven AI (2016). Bazı Antepfıstığı Çeşitlerinde Periyodisite ile Yaprak ve Meyvelerdeki Karbonhidrat Düzeyleri Arasındaki İlişkiler. Bahçe (Atatürk Bahçe Kültürleri Merkez Araştırma Enstitüsü Dergisi) Özel Sayı. VII. Ulusal Bahçe Bitkileri Kongresi Bildirileri Cilt: 45 Özel Sayı, S: 1117- 1121 (in Turkish).
  • Chiwocha S, von Aderkas P (2002). Endogenous levels of free and conjugated forms of auxin, cytokinins and abscisic acid during seed development in Douglas fir. Plant Growth Regulation 36 (3): 191-200.
  • Chiwocha SDS, Abrams SR, Ambrose SJ, Cutler AJ, Loewen M et al. (2003). A method for profiling classes of plant hormones and their metabolites using liquid chromatography-electrospray ionization tandem mass spectrometry: analysis of hormone regulation of thermodormancy of lettuce (Lactuca sativa L.) seeds. The Plant Journal 35 (3): 405-417.
  • Chiwocha SDS, Cutler AJ, Abrams SR, Ambrose SJ, Yang J et al. (2005). The etr1–2 mutation in Arabidopsis thaliana affects the abscisic acid, auxin, cytokinin and gibberellin metabolic pathways during maintenance of seed dormancy, moistchilling and germination. The Plant Journal 42 (1): 35-48.
  • Cohen JD (1982). Identification and quantitative analysis of indole3-acetyl-L-aspartate from seeds of Glycine max L. Plant Physiology 70 (3): 749-753.
  • Cohen JD, Bandurski RS (1982). Chemistry and physiology of the bound auxins. Annual Review of Plant Physiology 33 (1): 403- 430.
  • Crane JC, Al-Shalan I, Caresan R (1973). Abscission of pistachio inflorescence buds as effected by leaf area and number of nuts. Journal of the American Society for Horticultural Science 98: 591-592.
  • Crane JC, Iwakiri B (1987). Reconsideration of the cause of inflorescence bud abscission in pistachio. HortScience 22 (6): 1315-1316.
  • Crane JC, Nelson MM (1971). The unusual mechanism of alternate bearing in pistachio. HortScience 6: 489-490.
  • Davies PJ (1995). Plant Hormones: Physiology, Biochemistry and Molecular Biology. Kluwer Dordrecht, the Netherlands: Academic Publishers.
  • Davies PJ (2004). Plant hormones: their nature, occurrence and function. In: Davies PJ (editor). Plant Hormones: Biosynthesis, Signal Transduction, Action. 3rd ed. Dordrecht, the Netherlands: Kluwer Academic Publishers, pp. 1-15.
  • Davies PJ (2010). The Plant Hormones: Their Nature, Occurrence and Functions. 3rd ed. New York, NY, USA: Kluwer Academic, pp. 2-6.
  • Epstein E, Baldi BG, Cohen JD (1986). Identification of indole–3- acetyl glutamate from seeds of Glycine max L. Plant Physiology 80 (1): 256-258.
  • Ferguson L, Maranto J (1989). Effects of growth regulators on pistachio inflorescence and bud retention. California Pistachio Industry Annual Report Crop Year 1988–1989, pp. 91-92.
  • George EF, Michael Hall A, Klerk GD (2008). Plant Propagation by Tissue Culture. 3rd ed. The Background. Basingstone, UK: Exegetic.
  • Gundesli MA (2017). Determination of Mechanism of Bud Abscission in Pistachio. PhD, University of Çukurova, Institute of Natural and Applied Sciences.
  • Gündeşli MA, Kafkas S, Zarifikhosroshahi M, Kafkas NE (2019). Role of endogenous polyamines in the alternate bearing phenomenon in pistachio. Turkish Journal of Agriculture and Forestry 43: 265-274.
  • Güneş NT, Okay Y, Köksal AI, Köroğlu M (2010). The effect of nitrogen and phosphorus fertilization on yield, some fruit characteristics, hormone concentrations, and alternate bearing in pistachio. Turkish Journal of Agriculture and Forestry 34: 33-43.
  • Hoad GV (1983). Hormonal regulation of fruit-bud formation in fruit trees. Flowering and Fruit Set in Fruit Trees 149: 13-23.
  • Kai K, Horita J, Wakasa K, Miyagawa H (2007). Three oxidative metabolites of indole–3-acetic acid from Arabidopsis thaliana. Phytochemistry 68 (12): 1651-1663.
  • Kowalczyk M, Sandberg G (2001). Quantitative analysis of indole–3- acetic acid metabolites of Arabidopsis. Plant Physiology 127 (4): 1845-1853.
  • Lavee S (1989). Involvement of plant growth regulators and endogenous growth substances in the control of alternate bearing. Acta Horticulturae 239: 311-322.
  • Ljung K (2013). Auxin metabolism and homeostasis during plant development. Development 140 (5): 943-950.
  • Ljung K, Hull AK, Kowalczyk M, Marchant A, Celenza J et al. (2002). Biosynthesis, conjugation, catabolism and homeostasis of indole–3-acetic acid in Arabidopsis thaliana. In: Auxin Molecular Biology. Dordrecht, the Netherlands: Springer, pp. 249-272.
  • Lovatt CJ, Ferguson L (1998). Using foliar application of urea combined with 6-benzyladenin to decrease pistachio floral bud abscission in an ‘on’ year to increase yield the next year. California Pistachio Industry. Annual Report 1997–1998, pp. 155-158.
  • Lovatt CJ, Ferguson L (2001). Urea combined with 6-benzyladenin to reduce alternate bearing in pistachio and to increase cumulative yield (Fifth Year Report). California Pistachio Industr Annual Report 2000-2001, pp. 151-152.
  • Lu Q, Zhang L, Chen C, Lu M, Ping T et al. (2008). Identification and quantitation of auxins in plants by liquid chromatography/ electrospray ionization ion trap mass spectrometry. Rapid Communications in Mass Spectrometry: An International Journal Devoted to the Rapid Dissemination of Up‐to‐the‐ Minute Research in Mass Spectrometry 22 (16): 2565-2572.
  • Ludwig-Muller J (2011). Auxin conjugates: their role for plant development and in the evolution of land plants. Journal of Experimental Botany 62 (6): 1757-1773.
  • Ludwig-Muller J, Epstein E, Hilgenberg W (1996). Auxin-conjugate hydrolysis in Chinese cabbage: characterization of an amid hydrolase and its role during the club root disease. Physiologia Plantarum 97 (4): 627-634.
  • Lulsdorf MM, Yuan HY, Slater SM, Vandenberg A, Han X et al. (2013). Endogenous hormone profiles during early seed development of C. arietinum and C. anatolicum. Plant Growth Regulation 71 (2): 191-198.
  • Monselise SP, Goldschmidt E (1982). Alternate bearing in fruit tress: A review. Horticultural Reviews 4: 128-173.
  • Normanly J, Grisafi P, Fink GR, Bartel B (1997). Arabidopsis mutants resistant to the auxin effects of indole–3-acetonitrile are defective in the nitrilase encoded by the NIT1 gene. Plant Cell 9 (10): 1781-1790.
  • Nzima MDS, Martin GC, Nishijima C (1997). Seasonal changes in total nonstructural carbohydrates within branches and roots of naturally ‘off ’ and ‘on’ Kerman Pistachio trees. Journal of the American Society for Horticultural Science 122 (6): 856-862.
  • Okay Y, Gunes NT, Koksal IA (2011). Free endogenous growth regulators in Pistachio (Pistacia vera L.). African Journal of Agricultural Research 6 (5): 1161-1169.
  • Ostin A, Moritz T, Sandberg G (1992). Liquid chromatography/ mass spectrometry of conjugates and oxidative metabolites of indole‐3‐acetic acid. Biological Mass Spectrometry 21 (6): 292- 298.
  • Pencik A, Rolcik J, Novak O, Magnus V, Bartak P et al. (2009). Isolation of novel indole–3-acetic acid conjugates by immunoaffinity extraction. Talanta 80 (2): 651-655.
  • Piskornik A, Bandurski RS (1972). Purification and partial characterization of a glucan containing indole-3-acetic acid. Plant Physiology 50 (1): 176-182.
  • Porlingis IC (1974). Flower bud abscission in pistachio, as related to fruit development and other factors. Journal of the American Society for Horticultural Science 99: 121-125.
  • Prinsen E, Van Laer S, Oden S, Van Onckelen H (2000). Auxin analysis. In: Tucker GA, Roberts JA. (editors). Plant Hormone Protocols. Methods in Molecular Biology. Humana Press 141: 49-65.
  • Rampey RA, LeClere S, Kowalczyk M, Ljung K, Sandberg G et al. (2004). A family of auxin-conjugate hydrolases that contribute to free indole–3-acetic acid levels during Arabidopsis germination. Plant Physiology 135 (2): 978-988.
  • Ribnicky DM, Cooke TJ, Cohen JD (1998). A microtechnique for the analysis of free and conjugated indole–3-acetic acid in milligram amounts of plant tissue using a benchtop gas chromatograph-mass spectrometer. Planta 204 (1): 1-7.
  • Rosecrance RC, Weinbaum SA, Brown PH (1998). Alternate bearing affects nitrogen, phosphorus, potassium and starch storage pools in mature pistachio trees. Annals of Botany 82 (4): 463- 470.
  • Ruzicka K, Ljung K, Vanneste S, Podhorska R, Beeckman et al. (2007). Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell 19 (7): 2197-2212.
  • Sitbon F, Hennion S, Sundberg B, Little CHA, Olsson O et al. (1992). Transgenic tobacco plants coexpressing the Agrobacterium tumefaciens iaaM and iaaH genes display altered growth and indoleacetic acid metabolism. Plant Physiology 99 (3): 1062-1069.
  • Sonner JM, Purves WK (1985). Natural occurrence of indole–3-acetyl aspartate and indole–3-acetyl glutamate in cucumber shoot tissue. Plant Physiology 77 (3): 784-785.
  • Staswick PE, Serban B, Rowe M, Tiryaki I, Maldonado MT et al. (2005). Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole–3-acetic acid. The Plant Cell 17 (2): 616- 627.
  • Stevenson MT, Shackel KA (1998). Alternate bearing in pistachio as a masting phenomenon: Construction cost of reproduction versus vegetative growth and storage. Journal of the American Society for Horticultural Science 123: 1069-1075.
  • Takeda F, Ryugo K, Crane JC (1980). Translocation and distribution of 14C-photosynthates in bearing and nonbearing pistachio branches. Journal of the American Society for Horticultural Science 105 (5): 642-664.
  • Tam YY, Epstein E, Normanly J (2000). Characterization of auxin conjugates in Arabidopsis. Low steady-state levels of indole–3- acetyl-aspartate, indole–3-acetyl-glutamate, and indole–3-acetylglucose. Plant Physiology 123 (2): 589-595.
  • Tealei WD, Paponov IA, Palme K (2006). Auxin in action: signaling, transport and the control of plant growth and development. Nature Reviews Molecular Cell Biology 7 (11): 847-859.
  • Tivendale ND, Cohen JD (2015). Analytical History of Auxin. Plant Growth Regulation 34 (4): 708-722.
  • Vemmos SN (1999a). Carbohydrate content of inflorescent buds of defruited and fruiting pistachio (Pistacia vera L) branches in relation to biennial bearing. The Journal of Horticultural Science and Biotechnology 74 (1): 94-100.
  • Vemmos SN (1999b). Mineral composition of leaves and inflorescent buds in fruiting and non-fruiting pistachio trees. Journal of Plant Nutrition 22 (8): 1291-1301.
  • Vemmos SN, Pontikis CA, Tolia-Marioli AP (1994). Respiration rate and ethylene production in inflorescence buds of pistachio in relation to alternate bearing. Scientia Horticulturae 57 (1-2): 165-172.
  • Walz A, Park S, Slovin JP, Ludwig-Muller J, Momonoki YS et al. (2002). A gene encoding a protein modified by the phytohormone indoleacetic acid. Proceedings of the National Academy of Sciences 99 (3): 1718-1723.
  • Weinbaum S, Picchioni G, Muraoka T, Ferguson L, Brown P (1994). Fertilizer nitrogen and boron uptake, storage, and allocation vary during the alternate bearing cycle. Journal of the American Society for Horticultural Science 119: 24-31.
  • Zaharia LI, Galka MM, Ambrose SJ, Abrams SR (2005). Preparation of deuterated abscisic acid metabolites for use in mass spectrometry and feeding studies. Journal of Labelled Compounds and Radiopharmaceuticals: The Official Journal of the International Isotope Society 48 (6): 435-445.