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Genes & Genomics

, Volume 41, Issue 11, pp 1241–1251 | Cite as

Validation of MADS-box genes from apple fruit pedicels during early fruit abscission by transcriptome analysis and real-time PCR

  • Seong Heo
  • Yong Suk ChungEmail author
Research Article

Abstract

Background

Fruit abscission in an isolated region called abscission zone (AZ) is regulated by several genes including JOINTLESS, MACROCALYX and SEPALLATA, MADS-box genes, in tomato.

Objective

The surviving central pedicels and the abscised lateral pedicels were examined in fruit clusters in order to investigate apple MADS-box genes from fruit pedicels of self-abscising apple ‘Saika’ during early fruit abscission.

Methods

After performing RNA-Seq, transcription profiling was conducted on the MADS-box genes from apple central and lateral pedicels. The JOINTLESS homolog of apple (MdJOINTLESS) was amplified using degenerate primers annealing to a highly conserved domain based on the orthologous genes of various crops, including JOINTLESS gene of tomato. The expression pattern of MdJOINTLESS was investigated in central and lateral pedicles by real-time PCR.

Results

Some homologs were found which similar to JOINTLESS, MACROCALYX and SEPALLATA of tomato MADS-box genes from transcriptome analysis and RACE. Using phylogenetic analyses with the MADS-box gene family, MdJOINTLESS was classified into the SHORT VEGETATIVE PHASE (SVP) clade that included Arabidopsis and other crops. The expression level of MdJOINTLESS in central pedicel was more than twice as high as that of lateral pedicel.

Conclusion

In the current study, we could find apple homologs of JOINTLESS, MACROCALYX, SEPALLATA, which were known to regulate pedicel AZ development in tomato. Furthermore, MdJOINTLESS might contribute to auxin gradation, influencing hierarchical ranking of auxin transport between fruit pedicels of self-abscising apple.

Keywords

Malus × domestica Abscission zone Self-abscission MADS-box Transcriptome analysis 

Notes

Acknowledgements

This work was supported by the education, research and student guidance grant funded by Jeju National University in 2019.

Compliance with ethical standards

Conflict of interest

Seong Heo and Yong Suk Chung declare that they have no conflict of interest.

Research involving human and animal participants

This article does not contain any studies with human subjects or animals performed by any of the authors.

References

  1. Bangerth F (2000) Abscission and thinning of young fruit and their regulation by plant hormones and bioregulators. Plant Growth Regul 31:43–59Google Scholar
  2. Basu MM, González-Carranza ZH, Azam-Ali S, Tang S, Shahid AA, Roberts JA (2013) The manipulation of auxin in the abscission zone cells of Arabidopsis flowers reveals that indoleacetic acid signaling is a prerequisite for organ shedding. Plant Physiol 162:96–106PubMedPubMedCentralGoogle Scholar
  3. Belfield EJ, Ruperti B, Roberts JA, McQueen-Mason S (2005) Changes in expansin activity and gene expression during ethylene-promoted leaflet abscission in Sambucus nigra. J Exp Bot 56:817–823PubMedGoogle Scholar
  4. Butenko MA, Patterson SE, Grini PE, Stenvik GE, Amundsen SS, Mandal A, Aalen RB (2003) INFLORESCENCE DEFICIENT IN ABSCISSION controls floral organ abscission in Arabidopsis and identifies a novel family of putative ligands in plants. Plant Cell 15:2296–2307PubMedPubMedCentralGoogle Scholar
  5. Celton JM, Dheilly E, Guillou MC, Simonneau F, Juchaux M, Costes E, Laurens F, Renou JP (2014) Additional amphivasal bundles in pedicel pith exacerbate central fruit dominance and induce self-thinning of lateral fruitlets in apple. Plant Physiol 164:1930–1951PubMedPubMedCentralGoogle Scholar
  6. Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11:113–116Google Scholar
  7. Cho HT, Cosgrove DJ (2000) Altered expression of expansin modulates leaf growth and pedicel abscission in Arabidopsis thaliana. Proc Natl Acad Sci USA 97:9783–9788PubMedGoogle Scholar
  8. Cho SK, Larue CT, Chevalier D, Wang H, Jinn TL, Zhang S, Walker JC (2008) Regulation of floral organ abscission in Arabidopsis thaliana. Proc Natl Acad Sci USA 105:15629–15634PubMedGoogle Scholar
  9. Dal Cin V, Barbaro E, Danesin M, Murayama H, Velasco R, Ramina A (2009a) Fruitlet abscission: a cDNA-AFLP approach to study genes differentially expressed during shedding of immature fruits reveals the involvement of a putative auxin hydrogen symporter in apple (Malus × domestica L. Borkh.). Gene 442:26–36Google Scholar
  10. Dal Cin V, Velasco R, Ramina A (2009b) Dominance induction of fruitlet shedding in Malus × domestica (L. Borkh.): molecular changes associated with polar auxin transport. BMC Plant Biol 9:139Google Scholar
  11. Gregis V, Andrés F, Sessa A, Guerra RF, Simonini S, Mateos JL, Torti S, Zambelli F, Prazzoli GM, Bjerkan KN, Grini PE, Pavesi G, Colombo L, Coupland G, Kater MM (2013) Identification of pathways directly regulated by SHORT VEGETATIVE PHASE during vegetative and reproductive development in Arabidopsis. Genome Biol 14:R56PubMedPubMedCentralGoogle Scholar
  12. Hartmann U, Hohmann S, Nettesheim K, Wisman E, Saedler H, Huijser P (2000) Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis. Plant J 21:351–360PubMedGoogle Scholar
  13. Heo S, Hwang JH, Kim D, Yu DJ, Lee HJ (2015) Classification of apple genetic resources using early fruit abscission pattern. J Am Pomol Soc 69:102–108Google Scholar
  14. Heo S, Hwang JH, Jun JH, Lee HJ (2016) Abscission-related genes revealed by RNA-Seq analysis using self-abscising apple (Malus × domestica). J Hortic Sci Biotechnol 91:271–278Google Scholar
  15. Jinn TL, Stone JM, Walker JC (2000) HAESA, an Arabidopsis leucine-rich repeat receptor kinase, controls floral organ abscission. Genes Dev 14:108–117PubMedPubMedCentralGoogle Scholar
  16. Konishi S, Izawa T, Lin SY, Ebana K, Fujuta Y, Sasaki T, Yano M (2006) An SNP caused loss of seed shattering during rice domestication. Science 312:1392–1396PubMedGoogle Scholar
  17. Koren D, Resnick N, Gati EM, Belausov E, Weininger S, Kapulnik Y, Koltai H (2013) Strigolactone signalling in the endodermis is sufficient to restore root responses and involves SHORT HYPOCOTYL 2 (SHY2) activity. New Phytol 198:866–874PubMedGoogle Scholar
  18. Lavenus J, Goh T, Roberts I, Guyomarc’h S, Lucas M, De Smet I, Fukaki H, Beeckman T, Bennett M, Laplaze L (2013) Lateral root development in Arabidopsis: fifty shades of auxin. Trends Plant Sci 18:450–458Google Scholar
  19. Li C, Zhou A, Sang T (2006) Rice domestication by reducing shattering. Science 311:1936–1939PubMedGoogle Scholar
  20. Li Z, Reighard GL, Abbott AG, Bielenberg DG (2009) Dormancy-associated MADS genes from the EVG locus of peach [Prunus persica (L.) Batsch] have distinct seasonal and photoperiodic expression patterns. J Exp Bot 60:3521–3530PubMedPubMedCentralGoogle Scholar
  21. Liu D, Wang D, Qin Z, Zhang D, Yin L, Wu L, Colasanti J, Li A, Mao L (2014) The SEPALLATA MADS-box protein SlMBP21 forms protein complexes with JOINTLESS and MACROCALYX as a transcription activator for development of the tomato flower abscission zone. Plant J 77:284–296PubMedGoogle Scholar
  22. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408Google Scholar
  23. Mao L, Begum D, Chuang HW, Budiman MA, Szymkowiak EJ, Irish EE, Wing RA (2000) JOINTLESS is a MADS-box gene controlling tomato flower abscission zone development. Nature 406:910–913PubMedGoogle Scholar
  24. McKim SM, Stenvik GE, Butenko MA, Kristiansen W, Cho SK, Hepworth SR, Aalen RB, Haughn GW (2008) The BLADE-ON-PETIOLE genes are essential for abscission zone formation in Arabidopsis. Development 135:1537–1546PubMedGoogle Scholar
  25. Meir S, Hunter DA, Chen JC, Halaly V, Reid MS (2006) Molecular changes occurring during acquisition of abscission competence following auxin depletion in Mirabilis jalapa. Plant Physiol 141:1604–1616PubMedPubMedCentralGoogle Scholar
  26. Meir S, Philosoph-Hadas S, Sundaresan S, Selvaraj KS, Burd S, Ophir R, Kochanek B, Reid MS, Jiang CZ, Lers A (2010) Microarray analysis of the abscission-related transcriptome in the tomato flower abscission zone in response to auxin depletion. Plant Physiol 154:1929–1956PubMedPubMedCentralGoogle Scholar
  27. Merelo P, Agustí J, Arbona V, Costa ML, Estornell LH, Gómez-Cadenas A, Coimbra S, Gómez MD, Pérez-Amador MA, Domingo C, Talón M, Tadeo FR (2017) Cell wall remodeling in abscission zone cells during ethylene-promoted fruit abscission in citrus. Front Plant Sci 8:126PubMedPubMedCentralGoogle Scholar
  28. Nakano T, Kimbara J, Fujisawa M, Kitagawa M, Ihashi N, Maeda H, Kasumi T, Ito Y (2012) MACROCALYX and JOINTLESS interact in the transcriptional regulation of tomato fruit abscission zone development. Plant Physiol 158:439–450PubMedGoogle Scholar
  29. Nakano T, Fujisawa M, Shima Y, Ito Y (2013) Expression profiling of tomato pre-abscission pedicels provides insights into abscission zone properties including competence to respond to abscission signals. BMC Plant Biol 9:13–40Google Scholar
  30. Nakano T, Kato H, Shima Y, Ito Y (2015) Apple SVP family MADS-box proteins and the tomato pedicel abscission zone regulator JOINTLESS have similar molecular activities. Plant Cell Physiol 56:1097–1106PubMedGoogle Scholar
  31. Okushima Y, Fukaki H, Onoda M, Theologis A, Tasaka M (2007) ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell 19:118–130PubMedPubMedCentralGoogle Scholar
  32. Patterson SE (2001) Cutting loose: abscission and dehiscence in Arabidopsis. Plant Physiol 126:494–500PubMedPubMedCentralGoogle Scholar
  33. Roberts JA, Elliott KA, Gonzalez-Carranza ZH (2002) Abscission, dehiscence, and other cell separation processes. Annu Rev Plant Biol 53:131–158PubMedGoogle Scholar
  34. Schumacher K, Schmitt T, Rossberg M, Schmitz G, Theres K (1999) The Lateral suppressor (Ls) gene of tomato encodes a new member of the VHIID protein family. Proc Natl Acad Sci USA 96:290–295PubMedGoogle Scholar
  35. Sexton R, Roberts JA (1982) Cell biology of abscission. Annu Rev Plant Physiol 33:133–162Google Scholar
  36. Shi CL, Stenvik GE, Vie AK, Bones AM, Pautot V, Proveniers M, Aalen RB, Butenko MA (2011) Arabidopsis class I KNOTTED-like homeobox proteins act downstream in the IDA-HAE/HSL2 floral abscission signaling pathway. Plant Cell 23:2553–2567PubMedPubMedCentralGoogle Scholar
  37. Stenvik GE, Tandstad NM, Guo Y, Shi CL, Kristiansen W, Holmgren A, Clark SE, Aalen RB, Butenko MA (2008) The EPIP peptide of INFLORESCENCE DEFICIENT IN ABSCISSION is sufficient to induce abscission in Arabidopsis through the receptor-like kinases HAESA and HAESA-LIKE2. Plant Cell 20:1805–1817PubMedPubMedCentralGoogle Scholar
  38. Sun L, Bukovac MJ, Forsline PL, van Nocker S (2009) Natural variation in fruit abscission-related traits in apple (Malus). Euphytica 165:55–67Google Scholar
  39. Sun CH, Yu JQ, Duan X, Wang JH, Zhang QY, Gu KD, Hu DG, Zheng CS (2018) The MADS transcription factor CmANR1 positively modulates root system development by directly regulating CmPIN2 in chrysanthemum. Hortic Res 5:52PubMedPubMedCentralGoogle Scholar
  40. Theissen G, Saedler H (2001) Floral quartets. Nature 409:469–471PubMedGoogle Scholar
  41. Van Nocker S (2009) Development of the abscission zone. Stewart Posthar Rev. 5:1–6Google Scholar
  42. Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D, Salvi S, Pindo M, Baldi P, Castelletti S, Cavaiuolo M, Coppola G, Costa F, Cova V, Dal Ri A, Goremykin V, Komjanc M, Longhi S, Magnago P, Malacarne G, Malnoy M, Micheletti D, Moretto M, Perazzolli M, Si-Ammour A, Vezzulli S, Zini E, Eldredge G, Fitzgerald LM, Gutin N, Lanchbury J, Macalma T, Mitchell JT, Reid J, Wardell B, Kodira C, Chen Z, Desany B, Niazi F, Palmer M, Koepke T, Jiwan D, Schaeffer S, Krishnan V, Wu C, Chu VT, King ST, Vick J, Tao Q, Mraz A, Stormo A, Stormo K, Bogden R, Ederle D, Stella A, Vecchietti A, Kater MM, Masiero S, Lasserre P, Lespinasse Y, Allan AC, Bus V, Chagné D, Crowhurst RN, Gleave AP, Lavezzo E, Fawcett JA, Proost S, Rouzé P, Sterck L, Toppo S, Lazzari B, Hellens RP, Durel CE, Gutin A, Bumgarner RE, Gardiner SE, Skolnick M, Egholm M, Van de Peer Y, Salamini F, Viola R (2010) The genome of the domesticated apple (Malus × domestica Borkh.). Nat Genet 42:833–839PubMedGoogle Scholar
  43. Weigel D (1995) The genetics of flower development: from floral induction to ovule morphogenesis. Annu Rev Genet 29:19–39PubMedGoogle Scholar
  44. Wu RM, Walton EF, Richardson AC, Wood M, Hellens RP, Varkonyi-Gasic E (2012) Conservation and divergence of four kiwifruit SVP-like MADS-box genes suggest distinct roles in kiwifruit bud dormancy and flowering. J Exp Bot 63:797–807PubMedGoogle Scholar
  45. Wu R, Tomes S, Karunairetnam S, Tustin SD, Hellens RP, Allan AC, Macknight RC, Varkonyi-Gasic E (2017) SVP-like MADS box genes control dormancy and budbreak in apple. Front Plant Sci 8:477PubMedPubMedCentralGoogle Scholar
  46. Yamane H, Ooka T, Jotatsu H, Hosaka Y, Sasaki R, Tao R (2011) Expressional regulation of PpDAM5 and PpDAM6, peach (Prunus persica) dormancy-associated MADS-box genes, by low temperature and dormancy-breaking reagent treatment. J Exp Bot 62:3481–3488PubMedPubMedCentralGoogle Scholar
  47. Yoon J, Cho LH, Antt HW, Koh HJ, An G (2017) KNOX protein OSH15 induces grain shattering by repressing lignin biosynthesis genes. Plant Physiol 174:312–325PubMedPubMedCentralGoogle Scholar
  48. Yu LH, Miao ZQ, Qi GF, Wu J, Cai XT, Mao JL, Xiang CB (2014) MADS-box transcription factor AGL21 regulates lateral root development and responds to multiple external and physiological signals. Mol Plant 7:1653–1669PubMedPubMedCentralGoogle Scholar
  49. Zhou Y, Lu D, Li C, Luo J, Zhu BF, Zhu J, Shangguan Y, Wang Z, Sang T, Zhou B, Han B (2012) Genetic control of seed shattering in rice by the APETALA2 transcription factor SHATTERING ABORTION1. Plant Cell 24:1034–1048PubMedPubMedCentralGoogle Scholar

Copyright information

© The Genetics Society of Korea 2019

Authors and Affiliations

  1. 1.Apple Research Institute, National Institute of Horticultural and Herbal ScienceRural Development AdministrationGunwiSouth Korea
  2. 2.Department of Plant ScienceSeoul National UniversitySeoulSouth Korea
  3. 3.Department of Plant Resources and EnvironmentJeju National UniversityJejuSouth Korea

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