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Physiology and Molecular Biology of Plants

, Volume 25, Issue 5, pp 1283–1299 | Cite as

Opposite physiological effects upon jasmonic acid and brassinosteroid treatment on laticifer proliferation and co-occurrence of differential expression of genes involved in vascular development in rubber tree

  • Poochita Arreewichit
  • Pakatorn Sae-Lim
  • Kanlaya Nirapathpongporn
  • Unchera Viboonjun
  • Panida Kongsawadworakul
  • Jarunya NarangajavanaEmail author
Research Article
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Abstract

During growth of woody plant-trunk, the secondary meristem functions in giving rise the xylem and phloem. Rubber tree (Hevea brasiliensis Muell. Arg.), in addition, contains laticifers (latex producing vessels) in the vicinity of phloem. Insights into regulatory mechanisms of gene networks underlying laticifer proliferation in rubber tree has remained very limited. The candidate vascular development-related genes were selected to investigate for expression profile in phloem and xylem tissues of high latex yield- and high wood yield-clones of rubber tree. The differential gene expression between the mature branch-xylem and -phloem tissues was clearly observed. The cis-regulatory motif analysis revealed the existent of putative jasmonic acid (JA)- and brassinosteroid (BR)-responsive regulatory motifs in promoter regions of these genes, and consequently the effect of exogenous application of JA, BR or their respective signaling inhibitors, on the formation of laticifers in rubber tree was demonstrated. Interestingly, the laticifer numbers were significantly increased in JA-treatment, correlated with up-regulation of phloem development-related genes in both rubber tree clones. On the contrary, the laticifers were decreased in BR-treatment accompanying by up-regulation of xylem development-related genes, especially in high wood yield-rubber tree clone. BR-inhibitor treatment also enhanced laticifer numbers, while JA-inhibitor suppressed laticifer differentiation. Taken together, this study unveils the molecular interplay between JA/BR on vascular development in rubber tree and how this impacts the appearance of laticifers in this plant. This process is vital for a better understanding on laticifer differentiation and its impact in the manipulation of wood and latex yield in rubber tree improvement program.

Keywords

Brassinosteroid Jasmonic acid Laticifer Rubber tree Vascular development-related gene 

Abbreviations

BL

Brassinolide

BR

Brassinosteroid

BRL3

BRASSINOSTEROID INSENSITIVE 1-like3

HB8

HOMEOBOX8

HCA2

HIGH CAMBIAL ACTIVITY

IBU

Ibuprofen

JA

Jasmonic acid

KAN1

KANADI1

LBD1

Lateral organ boundaries domain-containing protein 1-like

LOB

Lateral organ boundaries

MeJA

Methyl-jasmonate

PCZ

Propiconazole

VND7

VASCULAR-RELATED NAC-DOMAIN7

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Notes

Acknowledgements

This research was partially supported by the Center of Excellence on Agricultural Biotechnology, Science and Technology Postgraduate Education and Research Development Office, Office of Higher Education Commission, Ministry of Education (AG-BIO/PERDO-CHE) Grant Nos. AG-BIO/59-001-001, AG-BIO/61-001-005 and a Grant from Mahidol University. The authors thank Dr. Paweena Traiperm for technical support and instrument for histochemical study of the laticifer structure.

Author contributions

JN conceived and designed of the research. PA conducted main parts of the research and PS-L performed some bioinformatics. KN contributed rubber tree from the Rubber Research Institute of Thailand. JN, PK and UV provided technical support, analyzed and discussed the results. JN and PA wrote the manuscript. All authors read and approved the manuscript.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

12298_2019_686_MOESM1_ESM.pdf (1.9 mb)
Supplementary material 1 (PDF 1938 kb)
12298_2019_686_MOESM2_ESM.pdf (258 kb)
Supplementary material 2 (PDF 257 kb)

References

  1. Baima S, Nobili F, Sessa G, Lucchetti S, Ruberti I, Morelli G (1995) The expression of the Athb-8 homeobox gene is restricted to provascular cells in Arabidopsis thaliana. Development 121(12):4171PubMedGoogle Scholar
  2. Baima S, Possenti M, Matteucci A, Wisman E, Altamura MM, Ruberti I et al (2001) The Arabidopsis ATHB-8 HD-Zip protein acts as a differentiation-promoting transcription factor of the vascular meristems. Plant Physiol 126(2):643CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bonke M, Thitamadee S, Mahonen AP, Hauser MT, Helariutta Y (2003) APL regulates vascular tissue identity in Arabidopsis. Nature 426(6963):181–186CrossRefGoogle Scholar
  4. Caño-Delgado A, Yin Y, Yu C, Vafeados D, Mora-García S, Cheng JC et al (2004) BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development 131(21):5341CrossRefPubMedGoogle Scholar
  5. Castelblanque L, Balaguer B, Martí C, Rodríguez JJ, Orozco M, Vera P (2016) Novel insights into the organization of laticifer cells: a cell comprising a unified whole system. Plant Physiol 172:1032–1044PubMedPubMedCentralGoogle Scholar
  6. Chow CN, Zheng HQ, Wu NY, Chien CH, Huang HD, Lee TY et al (2016) PlantPAN 20: an update of plant promoter analysis navigator for reconstructing transcriptional regulatory networks in plants. Nucleic Acids Res 44(5):1154–1160CrossRefGoogle Scholar
  7. Donner TJ, Sherr I, Scarpella E (2009) Regulation of preprocambial cell state acquisition by auxin signaling in Arabidopsis. Development 136(19):3235CrossRefPubMedGoogle Scholar
  8. Elo A, Immanen J, Nieminen K, Helariutta Y (2009) Stem cell function during plant vascular development. Sem Cell Dev Biol 20(9):1097–1106CrossRefGoogle Scholar
  9. Emery JF, Floyd SK, Alvarez J, Eshed Y, Hawker NP, Izhaki A et al (2003) Radial patterning of arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr Biol 13(20):1768–1774CrossRefPubMedGoogle Scholar
  10. Endo H, Yamaguchi M, Tamura T, Nakano Y, Nishikubo N, Yoneda A et al (2015) Multiple classes of transcription factors regulate the expression of VASCULAR-RELATED NAC-DOMAIN7, a master switch of xylem vessel differentiation. Plant Cell Physiol 56(2):242–254CrossRefPubMedGoogle Scholar
  11. Eshed Y, Baum SF, Perea JV, Bowman JL (2001) Establishment of polarity in lateral organs of plants. Curr Biol 11(16):1251–1260CrossRefPubMedGoogle Scholar
  12. Etchells JP, Smit ME, Gaudinier A, Williams CJ, Brady SM (2016) A brief history of the TDIF-PXY signalling module: balancing meristem identity and differentiation during vascular development. New Phytolt 209(2):474–484CrossRefGoogle Scholar
  13. Gomez JB (1982) Anatomy of hevea and its influence on latex production. Malaysian Rubber Research and Development Board No. 7, ISBN 9797312Google Scholar
  14. González-García MP, Vilarrasa-Blasi J, Zhiponova M, Divol F, Mora-García S, Russinova E et al (2011) Brassinosteroids control meristem size by promoting cell cycle progression in Arabidopsis roots. Development 138(5):849CrossRefPubMedGoogle Scholar
  15. Guo Y, Qin G, Gu H, Qu LJ (2009) Dof56/HCA2, a Dof transcription factor gene, regulates interfascicular cambium formation and vascular tissue development in Arabidopsis. Plant Cell 21(11):3518–3534CrossRefPubMedPubMedCentralGoogle Scholar
  16. Guo D, Zhou Y, Li HL, Zhu JH, Wang Y, Chen XT et al (2017) Identification and characterization of the abscisic acid (ABA) receptor gene family and its expression in response to hormones in the rubber tree. Sci Rep 7:45157.  https://doi.org/10.1038/srep45157 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Hagel JM, Yeung EC, Facchini PJ (2008) Got milk? The secret life of laticifers. Trends Plant Sci 13(12):631–639CrossRefPubMedGoogle Scholar
  18. Hao BZ, Wu JL (2000) Laticifer Differentiation in Hevea brasiliensis: induction by exogenous jasmonic acid and linolenic acid. Ann Bot 85(1):37–43CrossRefGoogle Scholar
  19. Huang T, Harrar Y, Lin C, Reinhart B, Newell NR, Talavera-Rauh F et al (2014) Arabidopsis KANADI1 acts as a transcriptional repressor by interacting with a specific cis-element and regulates auxin biosynthesis, transport, and signaling in opposition to HD-ZIPIII factors. Plant Cell 26(1):246–262CrossRefPubMedPubMedCentralGoogle Scholar
  20. Ilegems M, Douet V, Meylan-Bettex M, Uyttewaal M, Brand L, Bowman JL et al (2010) Interplay of auxin, KANADI and class III HD-ZIP transcription factors in vascular tissue formation. Development 137(6):975CrossRefPubMedGoogle Scholar
  21. Iwasaki T, Shibaoka H (1991) Brassinosteroids act as regulators of tracheary-element differentiation in isolated zinnia mesophyll cells. Plant Cell Physiol 32(7):1007–1014CrossRefGoogle Scholar
  22. Kubo M, Udagawa M, Nishikubo N, Horiguchi G, Yamaguchi M, Ito J et al (2005) Transcription switches for protoxylem and metaxylem vessel formation. Genes Dev 19(16):1855–1860CrossRefPubMedPubMedCentralGoogle Scholar
  23. Laosombut T, Arreewichit P, Nirapathpongporn K, Traiperm P, Kongsawadworakul P, Viboonjun U et al (2016) Differential expression of methyl jasmonate-responsive genes correlates with laticifer vessel proliferation in phloem tissue of rubber tree (Hevea brasiliensis). J Plant Growth Regul 35(4):1049–1063CrossRefGoogle Scholar
  24. Li J, Chory J (1997) A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90(5):929–938CrossRefPubMedGoogle Scholar
  25. Loh SC, Thottathil GP, Othman AS (2016) Identification of differentially expressed genes and signalling pathways in bark of Hevea brasiliensis seedlings associated with secondary laticifer differentiation using gene expression microarray. Plant Physiol Biochem 107(6):45–55CrossRefPubMedGoogle Scholar
  26. Miyazawa Y, Nakajima N, Abe T, Sakai A, Fujioka S, Kawano S et al (2003) Activation of cell proliferation by brassinolide application in tobacco BY-2 cells: effects of brassinolide on cell multiplication, cell cycle related gene expression, and organellar DNA contents. J Exp Bot 54(393):2669–2678CrossRefPubMedGoogle Scholar
  27. Nagata N, Asami T, Yoshida S (2001) Brassinazole, an inhibitor of brassinosteroid biosynthesis, inhibits development of secondary xylem in cress plants (Lepidium sativum). Plant Cell Physiol 42(9):1006–1011CrossRefGoogle Scholar
  28. Nahar K, Kyndt T, Hause B, Hofte M, Gheysen G (2013) Brassinosteroids suppress rice defense against root-knot nematodes through antagonism with the jasmonate pathway. Mol Plant Microbe Interact 26(1):106–115CrossRefPubMedGoogle Scholar
  29. Nieminen K, Blomster T, Helariutta Y, Mähönen AP (2015) Vascular cambium development. Arabidopsis Book Am Soc Plant Biol 13:e0177CrossRefGoogle Scholar
  30. Offler CE, McCurdy DW, Patrick JW, Talbot M (2003) Transfer cells: cells specialized for a special purpose. Ann Rev Plant Biol 54(1):431–454CrossRefGoogle Scholar
  31. Ohashi-Ito K, Fukuda H (2003) HD-Zip III homeobox genes that include a novel member, ZeHB-13 (Zinnia)/ATHB-15 (Arabidopsis), are involved in procambium and xylem cell differentiation. Plant Cell Physiol 44(12):1350–1358CrossRefPubMedGoogle Scholar
  32. Ohashi-Ito K, Fukuda H (2014) Initiation of vascular development. Physiol Plant 151(2):142–146CrossRefPubMedGoogle Scholar
  33. Ohashi-Ito K, Demura T, Fukuda H (2002) Promotion of transcript accumulation of novel Zinnia immature xylem-specific HD-Zip III homeobox genes by brassinosteroids. Plant Cell Physiol 43(10):1146–1153CrossRefPubMedGoogle Scholar
  34. Peres ALGL, Soares JS, Tavares RG, Righetto G, Zullo MAT, Mandava NB, Menossi M (2019) Brassinosteroids, the sixth class of phytohormones: a molecular view from the discovery to hormonal interactions in plant development and stress adaptation. Int J Mol Sci 20:331.  https://doi.org/10.3390/ijms20020331 CrossRefPubMedCentralGoogle Scholar
  35. Saini S, Sharma I, Pati PK (2015) Versatile roles of brassinosteroid in plants in the context of its homoeostasis, signaling and crosstalks. Front Plant Sci 5:5.  https://doi.org/10.3389/fpls.2015.00950 CrossRefGoogle Scholar
  36. Salazar-Henao JE, Lehner R, Betegón-Putze I, Vilarrasa-Blasi J, Caño-Delgado AI (2016) BES1 regulates the localization of the brassinosteroid receptor BRL3 within the provascular tissue of the Arabidopsis primary root. J Exp Bot 67(17):4951–4961CrossRefPubMedPubMedCentralGoogle Scholar
  37. Sehr EM, Agusti J, Lehner R, Farmer EE, Schwarz M, Greb T (2010) Analysis of secondary growth in the Arabidopsis shoot reveals a positive role of jasmonate signalling in cambium formation. Plant J 63(5):811–822CrossRefPubMedPubMedCentralGoogle Scholar
  38. Smetana O, Mäkilä R, Lyu M, Amiryousefi A, Rodríguez FS, Sánchez F et al (2019) High levels of auxin signalling define the stem-cell organizer of the vascular cambium. Nature 565:485–489CrossRefPubMedGoogle Scholar
  39. Tan D, Sun X, Zhang J (2014) Age-dependent and jasmonic acid-induced laticifer-cell differentiation in anther callus cultures of rubber tree. Planta 240(2):337–344CrossRefPubMedGoogle Scholar
  40. Tan D, Hu X, Fu L, Kumpeangkeaw A, Ding Z, Sun X, Zhang J (2017) Comparative morphology and transcriptome analysis reveals distinct functions of the primary and secondary laticifer cells in the rubber tree. Sci Rep 7:3126CrossRefPubMedPubMedCentralGoogle Scholar
  41. Tang C, Huang D, Yang J, Liu S, Sakr S, Li H, Qin Y (2010) The sucrose transporter HbSUT3 plays an active role in sucrose loading to laticifer and rubber productivity in exploited trees of Hevea brasiliensis (para rubber tree). Plant Cell Env 33(10):1708–1720CrossRefGoogle Scholar
  42. Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Browse J (2007) JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448(7154):661–665CrossRefGoogle Scholar
  43. Tian WM, Yang SG, Shi MJ, Zhang SX, Wu JL (2015) Mechanical wounding-induced laticifer differentiation in rubber tree: an indicative role of dehydration, hydrogen peroxide, and jasmonates. J Plant Physiol 182(6):95–103CrossRefPubMedGoogle Scholar
  44. Wu S, Zhang S, Chao J, Deng X, Chen Y, Shi M, Tian WM (2016) Transcriptome analysis of the signalling networks in coronatine-induced secondary laticifer differentiation from vascular cambia in rubber trees. Sci Rep 6:36384CrossRefPubMedPubMedCentralGoogle Scholar
  45. Xie Y, Straub D, Eguen T, Brandt R, Stahl M, Martínez-García JF et al (2015) Meta-analysis of arabidopsis KANADI1 direct target genes identifies a basic growth-promoting module acting upstream of hormonal signaling pathways. Plant Physiol 169(2):1240–1253CrossRefPubMedPubMedCentralGoogle Scholar
  46. Xu P, Kong Y, Li X, Li L (2013) Identification of molecular processes needed for vascular formation through transcriptome analysis of different vascular systems. BMC Genom 14:217CrossRefGoogle Scholar
  47. Yamaguchi M, Mitsuda N, Ohtani M, Ohme-Takagi M, Kato K, Demura T (2011) Vascular-related NAC-domain 7 directly regulates a broad range of genes for xylem vessel differentiation. BMC Proc 5(Suppl 7):O37CrossRefPubMedCentralGoogle Scholar
  48. Ye ZH (2002) Vascular tissue differentiation and pattern formation in plants. Ann Rev Plant Biol 53(1):183–202CrossRefGoogle Scholar
  49. Yordanov YS, Regan S, Busov V (2010) Members of the LATERAL ORGAN BOUNDARIES DOMAIN transcription factor family are involved in the regulation of secondary growth in populus. Plant Cell 22(11):3662–3677CrossRefPubMedPubMedCentralGoogle Scholar
  50. Zhang S, Tian SW (2016) The secondary laticifer differentiation in rubber tree is induced by trichostatin A, an inhibitor of histone acetylation. Front Agric Sci Eng 3(4):357–362CrossRefGoogle Scholar
  51. Zhang SX, Wu SH, Chen YY, Tian WM (2015) Analysis of differentially expressed genes associated with coronatine-induced laticifer differentiation in the rubber tree by subtractive hybridization suppression. PLoS ONE 10(7):e0132070CrossRefPubMedPubMedCentralGoogle Scholar
  52. Zhu Z, An F, Feng Y, Li P, Xue L, Guo H (2011) Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis. Proc Nat Acad Sci USA 108(30):12539–12544CrossRefPubMedGoogle Scholar

Copyright information

© Prof. H.S. Srivastava Foundation for Science and Society 2019

Authors and Affiliations

  • Poochita Arreewichit
    • 1
    • 2
  • Pakatorn Sae-Lim
    • 1
    • 2
  • Kanlaya Nirapathpongporn
    • 3
  • Unchera Viboonjun
    • 4
  • Panida Kongsawadworakul
    • 4
  • Jarunya Narangajavana
    • 1
    • 2
    Email author
  1. 1.Department of Biotechnology, Faculty of ScienceMahidol UniversityBangkokThailand
  2. 2.Center of Excellence on Agricultural Biotechnology: (AG-BIO/PERDO-CHE)BangkokThailand
  3. 3.Rubber Research Institute of Thailand (RRIT)BangkokThailand
  4. 4.Department of Plant Science, Faculty of ScienceMahidol UniversityPhayathai, BangkokThailand

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