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Isolation of a novel cell wall architecture mutant of rice with defective Arabidopsis COBL4 ortholog BC1 required for regulated deposition of secondary cell wall components

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Abstract

The plant secondary cell wall is a highly ordered structure composed of various polysaccharides, phenolic components and proteins. Its coordinated regulation of a number of complex metabolic pathways and assembly has not been resolved. To understand the molecular mechanisms that regulate secondary cell wall synthesis, we isolated a novel rice mutant, cell wall architecture1 (cwa1), that exhibits an irregular thickening pattern in the secondary cell wall of sclerenchyma, as well as culm brittleness and reduced cellulose content in mature internodes. Light and transmission electron microscopy revealed that the cwa1 mutant plant has regions of local aggregation in the secondary cell walls of the cortical fibers in its internodes, showing uneven thickness. Ultraviolet microscopic observation indicated that localization of cell wall phenolic components was perturbed and that these components abundantly deposited at the aggregated cell wall regions in sclerenchyma. Therefore, regulation of deposition and assembly of secondary cell wall materials, i.e. phenolic components, appear to be disturbed by mutation of the cwa1 gene. Genetic analysis showed that cwa1 is allelic to brittle culm1 (bc1), which encodes the glycosylphosphatidylinositol-anchored COBRA-like protein specifically in plants. BC1 is known as a regulator that controls the culm mechanical strength and cellulose content in the secondary cell walls of sclerenchyma, but the precise function of BC1 has not been resolved. Our results suggest that CWA1/BC1 has an essential role in assembling cell wall constituents at their appropriate sites, thereby enabling synthesis of solid and flexible internodes in rice.

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Abbreviations

AGP:

Arabinogalactan protein

bc :

brittle culm

Bk2 :

Brittle Stalk2

CesA:

Cellulose synthase catalytic subunit

COBL4:

COBRA-LIKE4

cwa1 :

cell wall architecture1

GFP:

Green fluorescent protein

GPI:

Glycosylphosphatidylinositol

irx :

irregular xylem

PNT1:

PEANUT1

SEM:

Scanning electron microscopy

TEM:

Transmission electron microscopy

UV:

Ultraviolet

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Acknowledgments

We thank Hikaru Sato (Graduate School of Bioresource and Bioenvironmental Sciences, Kyushu University, Fukuoka, Japan) for providing the rice mutants, and Yasuo Niwa (Graduate School of Nutritional and Environmental Sciences, University of Shizuoka, Shizuoka, Japan) for providing the sGFP gene.

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Authors and Affiliations

  1. Graduate School of Bio-Applications and Systems Engineering, Tokyo University of Agriculture and Technology, Koganei, 184-8588, Japan

    Kanna Sato, Ryu Suzuki, Nobuyuki Nishikubo, Sachi Takenouchi, Sachiko Ito, Yoshimi Nakano & Shinya Kajita

  2. College of Bioresource Science, Nihon University, 1866 Kameino, Fujisawa, Kanagawa, 252-0880, Japan

    Yoshihiro Katayama

  3. Forestry Research Institute, Oji Paper Co. Ltd, 24-9 Nobono-cho, Kameyama, Mie, 519-0212, Japan

    Nobuyuki Nishikubo

  4. Graduate School of Agriculture, Tokyo University of Agriculture and Technology, Fuchu, 183-8538, Japan

    Satoshi Nakaba & Ryo Funada

  5. Graduate School of Agriculture, Hokkaido University, Sapporo, 060-8589, Japan

    Yuzou Sano

  6. Bioscience and Biotechnology Center, Nagoya University, Nagoya, 464-8601, Japan

    Hidemi Kitano

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  1. Kanna Sato
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  2. Ryu Suzuki
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  3. Nobuyuki Nishikubo
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  6. Yoshimi Nakano
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  7. Satoshi Nakaba
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  8. Yuzou Sano
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  9. Ryo Funada
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  10. Shinya Kajita
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  12. Yoshihiro Katayama
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Corresponding authors

Correspondence to Kanna Sato or Yoshihiro Katayama.

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Sato, K., Suzuki, R., Nishikubo, N. et al. Isolation of a novel cell wall architecture mutant of rice with defective Arabidopsis COBL4 ortholog BC1 required for regulated deposition of secondary cell wall components. Planta 232, 257–270 (2010). https://doi.org/10.1007/s00425-010-1171-4

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