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Brassinosteroids facilitate xylem differentiation and wood formation in tomato

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Abstract

Main conclusion

BR signaling pathways facilitate xylem differentiation and wood formation by fine tuning SlBZR1/SlBZR2-mediated gene expression networks involved in plant secondary growth.

Brassinosteroid (BR) signaling and BR crosstalk with diverse signaling cues are involved in the pleiotropic regulation of plant growth and development. Recent studies reported the critical roles of BR biosynthesis and signaling in vascular bundle development and plant secondary growth; however, the molecular bases of these roles are unclear. Here, we performed comparative physiological and anatomical analyses of shoot morphological growth in a cultivated wild-type tomato (Solanum lycopersicum cv. BGA) and a BR biosynthetic mutant [Micro Tom (MT)]. We observed that the canonical BR signaling pathway was essential for xylem differentiation and sequential wood formation by facilitating plant secondary growth. The gradual retardation of xylem development phenotypes during shoot vegetative growth in the BR-deficient MT tomato mutant recovered completely in response to exogenous BR treatment or genetic complementation of the BR biosynthetic DWARF (D) gene. By contrast, overexpression of the tomato Glycogen synthase kinase 3 (SlGSK3) or CRISPR-Cas9 (CR)-mediated knockout of the tomato Brassinosteroid-insensitive 1 (SlBRI1) impaired BR signaling and resulted in severely defective xylem differentiation and secondary growth. Genetic modulation of the transcriptional activity of the tomato Brassinazole-resistant 1/2 (SlBZR1/SlBZR2) confirmed the positive roles of BR signaling pathways for xylem differentiation and secondary growth. Our data indicate that BR signaling pathways directly promote xylem differentiation and wood formation by canonical BR-activated SlBZR1/SlBZR2.

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Abbreviations

BR:

Brassionsteroids

MT:

Micro Tom

BZR1/2:

Brassinazole-resistant 1/2

BIN2:

Brassinosteroid-insensitive 2

GSK3:

Glycogen synthase kinase 3

BES1:

BRI1-EMS-suppressor 1

SCW:

Secondary cell wall

CR:

CRISPR-CAS9

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Acknowledgements

This work was carried out with the support of the Basic Science Research Program through the National Research Foundation of Korea (2015R1A4A1041869), Korean Ministry of Science, ICT and Future Planning, and the Next-Generation BioGreen 21 Program (no. PJ01313601), Rural Development Administration, Republic of Korea. SJP was supported by a grant from the National Research Foundation (2017R1A4A1015594) funded by the Korean Ministry of Science, ICT and Future Planning.

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Authors and Affiliations

  1. Department of Biology, Chungbuk National University, Cheongju, 28644, Republic of Korea

    Jinsu Lee, Hwa-Yong Lee, Kyunghwan Kim & Hojin Ryu

  2. National Agrobiodiversity Center, National Academy of Agricultural Science RDA, Jeonju, 54875, Republic of Korea

    Seahee Han

  3. Department of Information and Statistics, Chungbuk National University, Cheongju, 28644, Republic of Korea

    Bomi Jeong & Tae-Young Heo

  4. Department of Industrial Plant Science and Technology, Chungbuk National University, Cheongju, 28644, Republic of Korea

    Tae Kyung Hyun

  5. Department of Horticultural Bioscience, College of Natural Resource and Life Science, Pusan National University, Miryang, 50467, Republic of Korea

    Byoung Il Je

  6. Department of Biotechnology, Duksung Women’s University, Seoul, 01369, Republic of Korea

    Horim Lee

  7. Department of Forest Bio-Resources, National Institute of Forest Science, Suwon, 16631, Republic of Korea

    Donghwan Shim

  8. Division of Biological Sciences, Research Institute for Basic Science, Wonkwang University, Iksan, 54538, Republic of Korea

    Soon Ju Park

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  1. Jinsu Lee
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Lee, J., Han, S., Lee, HY. et al. Brassinosteroids facilitate xylem differentiation and wood formation in tomato. Planta 249, 1391–1403 (2019). https://doi.org/10.1007/s00425-019-03094-6

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