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.
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- 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.