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Journal of Plant Research

, Volume 132, Issue 1, pp 145–154 | Cite as

A cell-wall protein SRPP provides physiological integrity to the Arabidopsis seed

  • Hiroshi Uno
  • Natsuki Tanaka-Takada
  • Momoko Hattori
  • Mayu Fukuda
  • Masayoshi MaeshimaEmail author
Regular Paper
  • 83 Downloads

Abstract

Seed and root hair protective protein (SRPP) is expressed in seeds and root hairs, localized in the cell wall, and involved in cell wall integrity. We analyzed a loss-of-function mutant of SRPP, focusing on siliques and seeds. The srpp-1 plants generated dark brown shrunken seeds at a high rate. The germination rate of these defect seeds of srpp-1 was less than 6%, although apparently normal srpp-1 seeds germinated at a rate of 83%. The production ratio of severe phenotypic seeds was dependent on the growth conditions. When the srpp-1 plants were cultivated at low humidity, the defect ratio was 73%, which was significantly higher than that at normal humidity. Defects of the silique and seeds could be detected on day 7 after pollination and the apical region of the siliques displayed a severe phenotype at a high frequency. Complementation with an SRPP gene under the control of promoters specific to the embryo, seed coat, or valve (carpel) partially rescued the phenotype, and complementation using the SRPP promoter fully rescued the phenotype. Furthermore, overexpression of SRPP enhanced the thermotolerance. After the treatment of seeds at 50 °C for 2 h, the germination rate of the seeds from overexpression with the 35S promoter increased to levels twice that of the wild-type seeds. Under the same conditions, no srpp-1 seeds germinated. These results indicate that SRPP is essential for the production of normal viable seeds in siliques under stress conditions. It is possible that modification of the SRPP gene improves seed integrity.

Keywords

Arabidopsis thaliana Cell wall Seed development Seed viability SRPP 

Notes

Acknowledgements

We are grateful to Yoichi Nakanishi, Miki Kawachi, and Shoji Segami (Nagoya University, Japan) for their valuable advice. Observations by low-vacuum SEM were conducted with help from Takao Oi. We would also like to thank the Riken Bioresource Center (Tsukuba, Japan) for delivering the seeds of the srpp-1 mutant (RATM13-5238-1).

Funding

This work was supported by Japan Society for the Promotion of Science (JSPS) Grants-in-Aid for Scientific Research [KAKENHI, grant numbers 26252011 and 26113506 to M.M.], and by a Grant-in-Aid for JSPS Fellows (no. 26002201 to N.T.-T.).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10265_2018_1083_MOESM1_ESM.pdf (4.3 mb)
Supplementary material 1 (PDF 4450 KB)

References

  1. Alexandrov VY (1994) Functional aspects of cell response to heat shock. Int Rev Cytol 148:171–227CrossRefGoogle Scholar
  2. Beeckman T, de Rycke R, Viane R, Inze D (2000) Histological study of seed coat development in Arabidopsis thaliana. J Plant Res 113:139–148CrossRefGoogle Scholar
  3. Bernhardt C, Tierney M (2000) Expression of AtPRP3, a proline-rich structural cell wall protein from Arabidopsis, is regulated by cell-type-specific developmental pathways involved in root hair formation. Plant Physiol 122:705–714CrossRefGoogle Scholar
  4. Chen LQ, Lin IW, Qu XQ, Sosso D, McFarlane HE, Londoño A, Samuels AL, Frommer WB (2015) A cascade of sequentially expressed sucrose transporters in the seed coat and endosperm provides nutrition for the Arabidopsis embryo. Plant Cell 27:607–619CrossRefGoogle Scholar
  5. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743CrossRefGoogle Scholar
  6. Daher FB, Braybrook SA (2015) How to let go: pectin and plant cell adhesion. Front Plant Sci 6:523CrossRefGoogle Scholar
  7. Esfandiari E, Jin Z, Abdeen A, Griffiths JS, Western TL, Haughn GW (2013) Identification and analysis of an outer-seed-coat-specific promoter from Arabidopsis thaliana. Plant Mol Biol 81:93–104CrossRefGoogle Scholar
  8. Fowler TJ, Bernhardt C, Tierney ML (1999) Characterization and expression of four proline-rich cell wall protein genes in Arabidopsis encoding two distinct subsets of multiple domain proteins 1. Plant Physiol 121:1081–1091CrossRefGoogle Scholar
  9. Haughn G, Chaudhury A (2005) Genetic analysis of seed coat development in Arabidopsis. Trends Plant Sci 10:472–777CrossRefGoogle Scholar
  10. Hongo S, Sato K, Yokoyama R, Nishitani K (2012) Demethylesterification of the primary wall by PECTIN METHYLESTERASE35 provides mechanical support to the Arabidopsis stem. Plant Cell 24:2624–2634CrossRefGoogle Scholar
  11. Huang YC, Wu HC, Wang YD, Liu CH, Lin CC, Luo DL, Jinn TL (2017) PECTIN METHYLESTERASE34 contributes to heat tolerance through its role in promoting stomatal movement. Plant Physiol 174:748–763CrossRefGoogle Scholar
  12. Jeong HJ, Choi JY, Shin HY, Bae JM, Shin JS (2014) Seed-specific expression of seven Arabidopsis promoters. Gene 553:17–23CrossRefGoogle Scholar
  13. Lindstrom JT, Vodkin LO (1991) A soybean cell wall protein is affected by seed color genotype. Plant Cell 3:561–571CrossRefGoogle Scholar
  14. Louvet R, Cavel E, Guénin LGS, Roger D, Guerineau FGF, Pelloux J (2006) Comprehensive expression profiling of the pectin methylesterase gene family during silique development in Arabidopsis thaliana. Planta 224:782–791CrossRefGoogle Scholar
  15. Mao G, Wang R, Guan Y, Liu Y, Zhang S (2011) Sulfurtransferases 1 and 2 play essential roles in embryo and seed development in Arabidopsis thaliana. J Biol Chem 286:7548–7557CrossRefGoogle Scholar
  16. Mazzeo MF, Cacace G, Iovieno P, Massarelli I, Grillo S, Siciliano RA (2018) Response mechanisms induced by exposure to high temperature in anthers from thermo-tolerant and thermo-sensitive tomato plants: a proteomic perspective. PLoS ONE 13:e0201027CrossRefGoogle Scholar
  17. Müller K, Levesque-Tremblay G, Bartels S, Weitbrecht K, Wormit A, Usadel B, Haughn G, Kermode AR (2013) Demethylesterification of cell wall pectins in Arabidopsis plays a role in seed germination. Plant Physiol 161:305–316CrossRefGoogle Scholar
  18. Nakagawa T, Suzuki T, Murata S, Nakamura S, Hino T, Maeo K, Tabata R, Kawai T, Niwa Y, Watanabe Y, Nakamura K, Kimura T, Ishiguro S (2007) Improved gateway binary vectors: high performance vectors for creation of fusion constructs in transgenic analysis of plants. Biosci Biotech Biochem 71:2095–2100CrossRefGoogle Scholar
  19. Park CP, Seo YS (2015) Heat shock proteins: a review of the molecular chaperones for plant immunity. Plant Pathol J 31:323–333CrossRefGoogle Scholar
  20. Rajjou L, Debeaujon I (2008) Seed longevity: survival and maintenance of high germination ability of dry seeds. C R Biol 331:796–805CrossRefGoogle Scholar
  21. Raviv B, Aghajanyan L, Granot G, Makover V, Frenkel O, Gutterman Y, Grafi G (2017) The dead seed coat functions as a long-term storage for active hydrolytic enzymes. PLoS ONE 12:e0181102CrossRefGoogle Scholar
  22. Ripoll JJ, Bailey LJ, Mai QA, Wu SL, Hon CT, Chapman EJ, Ditta GS, Estelle M, Yanofsky MF (2015) MicroRNA regulation of fruit growth. Nat Plants 1:15036CrossRefGoogle Scholar
  23. Silva-Correia J, Freitas S, Tavares RM, Lino-Neto T, Azevedo H (2014) Phenotypic analysis of the Arabidopsis heat stress response during germination and early seedling development. Plant Methods 10:7CrossRefGoogle Scholar
  24. Tanaka N, Kato M, Tomioka R, Kurata R, Fukao Y, Aoyama T, Maeshima M (2014) Characteristics of a root hair-less line of Arabidopsis thaliana under physiological stresses. J Exp Bot 65:1497–1512CrossRefGoogle Scholar
  25. Tanaka N, Uno H, Okuda S, Gunji S, Ferjani A, Aoyama T, Maeshima M (2017) SRPP, a cell-wall protein involved in development and protection of seeds and root hairs in Arabidopsis thaliana. Plant Cell Physiol 58:760–769Google Scholar
  26. Uno H, Tanaka-Takada N, Sato R, Maeshima M (2017) Enhancement of cell wall protein SRPP expression during emergent root hair development in Arabidopsis. Plant Signal Behav 12:10–14CrossRefGoogle Scholar
  27. Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252CrossRefGoogle Scholar
  28. Wang M, Yuan D, Gao W, Li Y, Tan J, Zhang X (2013) A comparative genome analysis of PME and PMEI families reveals the evolution of pectin metabolism in plant cell walls. PLoS ONE 8:e72082CrossRefGoogle Scholar
  29. Wolf S, Greiner S (2012) Growth control by cell wall pectins. Protoplasma 249:S169–S175CrossRefGoogle Scholar
  30. Won SK, Lee YJ, Lee HY, Heo YK, Cho M, Cho HT (2009) Cis-element and transcriptome-based screening of root hair-specific genes and their functional characterization in Arabidopsis. Plant Physiol 150:1459–1473CrossRefGoogle Scholar
  31. Young TE, Ling J, Geisler-Lee CJ, Tanguary RL, Caldwell C, Gallie DR (2001) Developmental and thermal regulation of the maize heat shock protein, HSP101. Plant Physiol 127:777–791CrossRefGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan KK, part of Springer Nature 2019

Authors and Affiliations

  • Hiroshi Uno
    • 1
  • Natsuki Tanaka-Takada
    • 1
    • 2
  • Momoko Hattori
    • 1
  • Mayu Fukuda
    • 1
  • Masayoshi Maeshima
    • 1
    Email author
  1. 1.Laboratory of Cell Dynamics, Graduate School of Bioagricultural SciencesNagoya UniversityNagoyaJapan
  2. 2.Department of Plant SciencesUniversity of OxfordOxfordUK

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