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2022 Vol.40, Issue 5 Preview Page

Research Article

Exogenous Brassinosteroids Regulate Mango Fruit Set through Inflorescence Development and Pollen Fertility
Teerapat Tepkaew1
,
Ornusa Khamsuk1
,
Jenjira Chumpookam2
,
Weerasin Sonjaroon3
,
Kanapol Jutamanee1*
1Department of Botany, Faculty of Science, Kasetsart University, Bangkok 10900, Thailand
2Department of Horticulture, Faculty of Agriculture, Kasetsart University, Bangkok 10900, Thailand
3Kasetsart Agricultural and Agro-Industrial Product Improvement Institute, Kasetsart University, Bangkok 10900, Thailand
*Corresponding Author
31 October 2022. pp. 481-495
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Abstract

Fruit set reduction is currently an important issue with regard to mango cultivation due to pollen infertility. Brassinosteroids (BRs) reportedly promote plant reproductive development, which is considered to be a strategy for reducing fertilization failures due to infertile pollen. In this study, 24-epibrassinolide (EBR), a natural brassinosteroid, and 7,8-dihydro-8α-20-hydroxyecdysone (DHECD), a brassinosteroid mimic, were applied to mango inflorescence to evaluate the effects of EBR and DHECD on inflorescence bud development and pollen fertility. Both BRs were sprayed at amounts of 0.01 or 0.1 µM when the inflorescence buds had developed to the ‘large bud swell’ stage. The results demonstrated that exogenous DHECD and EBR improved inflorescence bud development and reduced the percentage of malformed inflorescence. Application of the BRs increased the inflorescence length, the total number of flowers per inflorescence, the pollen viability, and the fruit set level. In addition, DHECD enhanced pollen germination in the pistil by elevating the pollen enzyme activities of α-amylase, Ca2+-ATPase, and polymethylesterase. The 0.1 µM DHECD application effectively improved both inflorescence bud development and pollen enzyme activity. A certain concentration of DHECD showed potential similar to EBR. It was concluded that EBR and DHECD can play effective roles in regulating fruit set through pollen fertility and can help with the problem of low fruit set outcomes in mango.

Keywords
24-epibrassinolide
DHECD
Mangifera indica
pollen enzymes
pollen germination
pollen viability
References
1
Bosch M, Cheung AY, Hepler PK (2005) Pectin methylesterase, a regulator of pollen tube growth. Plant Physiol 138: 1334-1346. doi:10.1104/pp.105.059865 10.1104/pp.105.05986515951488PMC1176407
2
Calzoni GL, Speranza A (1982) Effect of methanol and gamma irradiation on enzymatic activity of apple pollen. Sci Hortic 17: 231-239. doi:10.1016/0304-4238(82)90045-0 10.1016/0304-4238(82)90045-0
3
Cieslak M, Owens A, Prusinkiewicz P (2022) Computational models of auxin-driven patterning in shoots. Cold Spring Harb Perspect Biol 14: a040097. doi:10.1101/cshperspect.a040097 10.1101/cshperspect.a04009734001531
4
Clouse SD, Zurek DM, McMorris TC, Baker ME (1992) Effect of brassinolide on gene expression in elongating soybean epicotyls. Plant Physiol 100: 1377-1383. 1992. doi:10.1104/pp.100.3.1377 10.1104/pp.100.3.137716653132PMC1075793
5
Cohen JD, Meudt WJ (1983) Investigations on the mechanism of the brassinosteroid response: I. Indole-3-acetic acid metabolism and transport. Plant Physiol 72: 691-694. doi:10.1104/pp.72.3.691 10.1104/pp.72.3.69116663068PMC1066303
6
Domagalska MA, Sarnowska E, Nagy F, Davis SJ (2010) Genetic analyses of interactions among gibberellin, abscisic acid, and brassinosteroids in the control of flowering time in Arabidopsis thaliana. PloS one 5: e14012, 2010. doi:10.1371/journal.pone.0014012 10.1371/journal.pone.001401221103336PMC2984439
7
Ferrie AMR, Dirpaul J, Krishna P, Krochko J, Keller WA (2005) Effects of brassinosteroids on microspore embryogenesis in Brassica species. In Vitro Cell Dev Biol Plant 41: 742-745. doi:10.1079/IVP2005690 10.1079/IVP2005690
8
Franklin-Tong VE (1999) Signaling and the modulation of pollen tube growth. Plant Cell 11: 727-738. doi:10.1105/tpc.11.4.727 10.1105/tpc.11.4.72710213789PMC144203
9
Gallego-Bartolomé J, Minguet EG, Grau-Enguix F, Abbas M, Locascio A, Thomas SG, Alabadí D, Blázquez MA (2012) Molecular mechanism for the interaction between gibberellin and brassinosteroid signaling pathways in Arabidopsis. Proc Natl Acad Sci USA 109: 13446-13451. doi:10.1073/pnas.1119992109 10.1073/pnas.111999210922847438PMC3421204
10
Genç AC (2019) The effect of brassinosteroid on pollen germination and tube growth in three Dianthus species. CBUJOS 15: 371-375. doi:10.18466/cbayarfbe.628874 10.18466/cbayarfbe.628874
11
Gökbayrak Z, Engin H (2016) Effect of plant growth regulators on in vitro pollen germination of grapevine cultivars. Acta Hortic 1139: 405-408. doi:10.17660/ActaHortic.2016.1139.70 10.17660/ActaHortic.2016.1139.70
12
Gökbayrak Z, Engin H (2018a) Effects of foliar-applied brassinosteroid on viability and in vitro germination of pollen collected from bisexual and functional male flowers of pomegranate. Int J Fruit Sci 18: 226-230. doi:10.1080/15538362.2018.1425652 10.1080/15538362.2018.1425652
13
Gökbayrak Z, Engin H (2018b) Influence of plant growth regulators on sex differentiation and floral characteristics of pomegranate flowers: a case of brassinosteroids. Acta Soc Bot Pol 87: 3589. doi:10.5586/asbp.3589 10.5586/asbp.3589
14
Guan YF, Guo JZ, Li H, Yang ZB (2013) Signaling in pollen tube growth: crosstalk, feedback, and missing links. Mol Plant 6: 1053-1064. doi:10.1093/mp/sst070 10.1093/mp/sst07023873928PMC3842152
15
Hagerman AE, Austin PJ (1986) Continuous spectrophotometric assay for plant pectin methyl esterase. J Agric Food Chem 34: 440-444. doi:10.1021/jf00069a015 10.1021/jf00069a015
16
Hayat S, Fariduddin Q, Ahmad A (2003) Homobrassinolide effects on germination and α-amylase activity in wheat seeds. Seed Technol 25: 45-49.
17
Herbell S, Gutermuth T, Konrad KR (2018) An interconnection between tip-focused Ca2+ and anion homeostasis controls pollen tube growth. Plant Signal Behav 13:e1529521. doi:10.1080/15592324.2018.1529521 10.1080/15592324.2018.152952130307369PMC6279333
18
Holá D, Rothová O, Kočová M, Kohout L, Kvasnica M (2010) The effect of brassinosteroids on the morphology, development and yield of field-grown maize. Plant Growth Regul 61: 29-43. doi:10.1007/s10725-010-9446-0 10.1007/s10725-010-9446-0
19
Huang G, Han M, Yao W, Wang Y (2017) Transcriptome analysis reveals the regulation of brassinosteroids on petal growth in Gerbera hybrida. PeerJ 5: e3382. doi:10.7717/peerj.3382 10.7717/peerj.338228584713PMC5455292
20
Kang JG, Yun J, Kim DH, Chung K, Fujioka S, Kim J, Dae H, Yoshida S, Takatsuto S, et al. (2001) Light and brassinosteroid signals are integrated via a dark-induced small G protein in etiolated seedling growth. Cell 105: 625-636. doi:10.1016/S0092-8674(01)00370-1 10.1016/S0092-8674(01)00370-1
21
Kanwar MK, Bakshi P, Sharma P, Kour J, Singh AD, Dhiman S, Ibhrahim M, Mir BA, Ahammed GJ, et al. (2022) Brassinosteroids in plant reproductive development. In Yu JQ, Ahammed GJ, Krishna P, eds, Brassinosteroids in Plant Developmental Biology and Stress Tolerance. Academic Press, London, UK, pp 105-130. doi:10.1016/B978-0-12-813227-2.00009-6 10.1016/B978-0-12-813227-2.00009-6
22
Katsumi M (1985) Interaction of a brassinosteroid with IAA and GA3 in the elongation of cucumber hypocotyl sections. Plant Cell Physio l26:615-625. doi:10.1093/oxfordjournals.pcp.a076950 10.1093/oxfordjournals.pcp.a076950
23
Kearns CA, Inouye DW (1993) Techniques for Pollination Biologists. University Press of Colorado, Colorado, USA.
24
Kermanee P (2008) Plant Microtechnique, Kasetsart University Press, Bangkok, Thailand.
25
Khamsuk O, Sonjaroon W, Suwanwong S, Jutamanee K, Suksamrarn A (2018) Effects of 24-epibrassinolide and the synthetic brassinosteroid mimic on chili pepper under drought. Acta Physiol Plant 40: 1-12. doi:10.1007/s11738-018-2682-z 10.1007/s11738-018-2682-z
26
Li QF, Wang C, Jiang L, Li S, Sun SS, He JX (2012) An interaction between BZR1 and DELLAs mediates direct signaling crosstalk between brassinosteroids and gibberellins in Arabidopsis. Sci Signal 5: ra72. doi:10.1126/scisignal.2002908 10.1126/scisignal.2002908
27
Li Z, He Y (2020) Roles of brassinosteroids in plant reproduction. Int J Mol Sci 21: 872. doi:10.3390/ijms21030872 10.3390/ijms2103087232013254PMC7037687
28
Maneechote P, Saeng-ngam S, Chaivisuthangkura P (2020) Effect of 7,8-dihydro-8α-20-hydroxyecdysone on photosynthesis, chlorophyll content and chloroplast structure in tomato (Solanum lycopersicum cv."CH154") under drought stress. ASEAN J Sci Technol Dev 23: 14-23
29
Manzano S, Martínez C, Megías Z, Gómez P, Garrido D, Jamilena M (2011) The role of ethylene and brassinosteroids in the control of sex expression and flower development in Cucurbita pepo. Plant Growth Regul 65: 213-221. doi:10.1007/s10725-011-9589-7 10.1007/s10725-011-9589-7
30
Nie S, Huang S, Wang S, Cheng D, Liu J, Lv S, Li Q, Wang X (2017) Enhancing brassinosteroid signaling via overexpression of tomato (Solanum lycopersicum) SlBRI1 improves major agronomic traits. Front Plant Sci 8: 1386. doi:10.3389/fpls.2017.01386 10.3389/fpls.2017.0138628848587PMC5554372
31
Nkansah GO, Ofosu-Amin J, Marouli A (2012) Gibberellic acid and Napthalene acetic acid affect fruit retention, yield and quality of Keitt mangoes in the coastal savanna ecological zone of Ghana. J Plant Physiol 7: 243-251. doi:10.3923/ajpp.2012.243.251 10.3923/ajpp.2012.243.251
32
Oosthuyse SA (1991) Stages of development of the mango panicle. S.A. Mango Growers Assoc Yearbook 11: 59-61
33
Peng J, Tang X, Feng H (2004) Effects of brassinolide on the physiological properties of litchi pericarp (Litchi chinensis cv. nuomoci). Sci Hortic 101: 407-416. doi:10.1016/j.scienta.2003.11.012 10.1016/j.scienta.2003.11.012
34
Planas-Riverola A, Gupta A, Betegón-Putze I, Bosch N, Ibañes M, Caño-Delgado AI (2019) Brassinosteroid signaling in plant development and adaptation to stress. Development 146: dev151894. doi:10.1242/dev.151894 10.1242/dev.15189430872266PMC6432667
35
Rick W, Stegbauer HP (1974) α-Amylase measurement of reducing groups. In Bergmeyer HU, ed, Methods of Enzymatic Analysis. Academic Press, USA, pp 885-890. doi:10.1016/B978-0-12-091302-2.50074-8 10.1016/B978-0-12-091302-2.50074-8
36
Roghabadi MA, Pakkish ZA (2014) Role of brassinosteroid on yield, fruit quality and postharvest storage of 'Tak Danehe Mashhad' sweet cherry (Prunus avium L.). Agricultural Communications 2: 49-56
37
Scheible N, McCubbin A (2019) Signaling in pollen tube growth: beyond the tip of the polarity iceberg. Plants 8: 156. doi:10.3390/plants8060156 10.3390/plants806015631181594PMC6630365
38
Schiøtt M, Romanowsky SM, Bækgaard L, Jakobsen MK, Palmgren MG, Harper JF (2004) A plant plasma membrane Ca2+ pump is required for normal pollen tube growth and fertilization. PNAS 101:9502-9507. doi:10.1073/pnas.0401542101 10.1073/pnas.040154210115197266PMC439006
39
Serna M, Hernández F, Coll F, Coll Y, Amorós A (2012) Brassinosteroid analogues effects on the yield and quality parameters of greenhouse-grown pepper (Capsicum annuum L.). Plant Growth Regul 68: 333-342. doi:10.1007/s10725-012-9718-y 10.1007/s10725-012-9718-y
40
Singh I, Shono M (2003) Effect of 24-epibrassinolide on pollen viability during heat-stress in tomato. - Indian J. Exp. Biol. 41: 174-176, 2003.
41
Singh I, Shono M (2005) Physiological and molecular effects of 24-epibrassinolide, a brassinosteroid on thermotolerance of tomato. Plant Growth Regul 47: 111-119. doi:10.1007/s10725-005-3252-0 10.1007/s10725-005-3252-0
42
Singh Z (2000) Hormonal physiology of mango malformation - an overview. Acta Hortic 525: 229-236. doi:10.17660/ActaHortic.2000.525.27 10.17660/ActaHortic.2000.525.27
43
Singh Z, Singh L (1995) Increased fruit set and retention in mango with exogenous application of polyamines. J Hortic Sci 70: 271-277. doi:10.1080/14620316.1995.11515297 10.1080/14620316.1995.11515297
44
Song YL, Dong YJ, Tian XY, Kong J, Bai XY, Xu LL, He ZL (2016) Role of foliar application of 24-epibrassinolide in response of peanut seedlings to iron deficiency. Biol Plant 60: 329-342. doi:10.1007/s10535-016-0596-4 10.1007/s10535-016-0596-4
45
Sonjaroon W, Jutamanee K, Khamsuk O, Thussagunpanit J, Kaveeta L, Suksamrarn A (2018) Impact of brassinosteroid mimic on photosynthesis, carbohydrate content and rice seed set at reproductive stage under heat stress. Agric Nat Resour 52: 234-240. doi:10.1016/j.anres.2018.09.001 10.1016/j.anres.2018.09.001
46
Straltsova D, Chykun P, Subramaniam S, Sosan A, Kolbanov D, Sokolik A, Demidchik V (2015) Cation channels are involved in brassinosteroid signalling in higher plants. Steroids 97: 98-106. doi:10.1016/j.steroids.2014.10.008 10.1016/j.steroids.2014.10.00825449770
47
Sukhvibul N, Whiley AW, Smith MK, Hetherington SE, Vithanage V (1999) Effect of temperature on inflorescence and floral development in four mango (Mangifera indica L.) cultivars. Sci Hortic 82: 67-84. doi:10.1016/S0304-4238(99)00041-2 10.1016/S0304-4238(99)00041-2
48
Suksamrarn A, Tanachatchairatana T, Sirigarn C (2002) Stereoselective catalytic hydrogenation of Δ7-6-ketosteroids in the presence of sodium nitrite. Tetrahedron 58: 6033-6037. doi:10.1016/S0040-4020(02)00580-X 10.1016/S0040-4020(02)00580-X
49
Szekeres M, Németh K, Koncz-Kálmán Z, Mathur J, Kauschmann A, Altmann T, Rédei GP, Nagy F, Schell J, et al. (1996) Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis. Cell 85: 171-182. doi:10.1016/S0092-8674(00)81094-6 10.1016/S0092-8674(00)81094-6
50
Thussagunpanit J, Jutamanee K, Kaveeta L, Chai-arree W, Pankean P, Suksamrarn A (2013) Effects of a brassinosteroid and an ecdysone analogue on pollen germination of rice under heat stress. Pestic Sci 38: 105-111. doi:10.1584/jpestics.D13-029 10.1584/jpestics.D13-029
51
Thussagunpanit J, Jutamanee K, Chai-arree W, Pankean P, Homvisasevongsa S, Suksamrarn A (2015) Comparative effects of brassinosteroid and brassinosteroid mimic on improving photosynthesis, lipid peroxidation, and rice seed set under heat stress. J Plant Growth Regul 34: 320-331. doi:10.1007/s00344-014-9467-4 10.1007/s00344-014-9467-4
52
Thussagunpanit J, Jutamanee K, Homvisasevongsa S, Suksamrarn A, Yamagami A, Nakano T, Asami T (2017) Characterization of synthetic ecdysteroid analogues as functional mimics of brassinosteroids in plant growth. J Steroid Biochem Mol Biol 172: 1−8. doi:10.1016/j.jsbmb.2017.05.003 10.1016/j.jsbmb.2017.05.00328479230
53
Vardhini BV, Rao SSR (1998) Effect of brassinosteroids on growth, metabolite content and yield of Arachis hypogaea. Phytochemistry 48: 927-930. doi:10.1016/S0031-9422(97)00710-3 10.1016/S0031-9422(97)00710-3
54
Vogler F, Schmalzl C, Englhart M, Bircheneder M, Sprunck S (2014) Brassinosteroids promote Arabidopsis pollen germination and growth. Plant Reprod 27: 153-167. doi:10.1007/s00497-014-0247-x 10.1007/s00497-014-0247-x25077683
55
Wang Q, Hasson A, Rossmann S, Theres K (2016) Divide et impera: boundaries shape the plant body and initiate new meristems. New Phytol 209: 485-498. doi:10.1111/nph.13641 10.1111/nph.1364126391543
56
Xiong M, Chu L, Li Q, Yu J, Yang Y, Zhou P, Zhou Y, Zhang C, Fan X, et al. (2021) Brassinosteroid and gibberellin coordinate rice seed germination and embryo growth by regulating glutelin mobilization. Crop J 9: 1039-1048. doi:10.1016/j.cj.2020.11.006 10.1016/j.cj.2020.11.006
57
Yan MY, Xie DL, Cao JJ, Xia XJ, Shi K, Zhou YH, Zhou J, Foyer CH, Yu JQ (2020) Brassinosteroid‐mediated reactive oxygen species are essential for tapetum degradation and pollen fertility in tomato. Plant J 102: 931-947. doi:10.1111/tpj.14672 10.1111/tpj.1467231908046
58
Ye Q, Zhua W, Li L, Zhang S, Yin Y, Ma H, Wang X (2010) Brassinosteroids control male fertility by regulating the expression of key genes involved in Arabidopsis anther and pollen development. PNAS 107: 6100-6105. doi:10.1073/pnas.0912333107 10.1073/pnas.091233310720231470PMC2851861
59
Zhang S, Wei Y, Lu Y, Wang X (2009) Mechanisms of brassinosteroids interacting with multiple hormones. Plant Signal Behav 4: 1117-1120. doi:10.4161/psb.4.12.9903 10.4161/psb.4.12.990320514225PMC2819435
60
Zhang Y, Li B, Xu Y, Li H, Li S, Zhang D, Mao Z, Guo S, Yang C, et al. (2013) The Cyclophilin CYP20-2 modulates the conformation of BRASSINAZOLE-RESISTANT1, which binds the promoter of FLOWERING LOCUS D to regulate flowering in Arabidopsis. The Plant Cell 25: 2504-2521. doi:10.1105/tpc.113.110296 10.1105/tpc.113.11029623897924PMC3753379
61
Zhu X, Liang W, Cui X, Chen M, Yin C, Luo Z, Zhu J, Lucas WJ, Wang Z, et al. (2015) Brassinosteroids promote development of rice pollen grains and seeds by triggering expression of carbon starved anther, a MYB domain protein. Plant J 82: 570-581. doi:10.1111/tpj.12820 10.1111/tpj.1282025754973
62
Zocca F, Lomolino G, Curioni A, Spettoli P, Lante A (2007) Detection of pectinmethylesterase activity in presence of methanol during grape pomace storage. Food Chem 102: 59-65. doi:10.1016/j.foodchem.2006.01.061 10.1016/j.foodchem.2006.01.061
Information
  • Publisher :KOREAN SOCIETY FOR HORTICULTURAL SCIENCE
  • Publisher(Ko) :원예과학기술지
  • Journal Title :Horticultural Science and Technology
  • Journal Title(Ko) :원예과학기술지
  • Volume : 40
  • No :5
  • Pages :481-495
  • Received Date : 2022-08-22
  • Revised Date : 2022-09-09
  • Accepted Date : 2022-09-14
  • DOI :https://doi.org/10.7235/HORT.20220043
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