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Improvement of cell wall digestibility in tall fescue by Oryza sativa SECONDARY WALL NAC DOMAIN PROTEIN2 chimeric repressor

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Abstract

Forage digestibility is one of the most important factors in livestock performance. As grasses grow and mature, dry matter increases but they become fibrous with secondary cell wall deposition and lignification of sclerenchyma cells, and forage quality drops. In rice (Oryza sativa), the SECONDARY WALL NAC DOMAIN PROTEIN2 fused with the modified EAR-like motif repression domain (OsSWN2-SRDX) reduces secondary cell wall thickening in sclerenchyma cells. We introduced OsSWN2-SRDX under the control of the OsSWN1 promoter into tall fescue (Festuca arundinacea Schreb.) to increase cell wall digestibility. Of 23 transgenic plants expressing OsSWN2-SRDX, nine had brittle internodes that were easily broken by bending. Their secondary cell walls were significantly thinner than those of the wild type in interfascicular fibers of internodes and in cortical fiber cells between leaf epidermal cells and vascular bundles. The dry matter digestibility increased by 11.8% in stems and by 6.8% in leaves compared with the wild type, and therefore forage quality was improved. In stem interfascicular fibers, acid detergent fiber and acid insoluble lignin were greatly reduced. Thus, the reduction of indigestible fiber composed of cellulose and lignin increased the degradability of sclerenchyma cell walls. OsSWN2-SRDX plants offer great potential in the genetic improvement of forage digestibility.

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References

  • Abe A (1988) Feed analyses based on the carbohydrates and its application to the nutritine value of feeds. Mem Nat Inst Anim Ind 2:1–75 (In Japanese)

    Google Scholar 

  • Casler MD, Vogel KP (1999) Accomplishments and impact from breeding for increased forage nutritional value. Crop Sci 39:12–20

    Article  Google Scholar 

  • Chai M, Bellizzi M, Wan C, Cui Z, Li Y, Wang G-L (2015) The NAC transcription factor OsSWN1 regulates secondary cell wall development in Oryza sativa. J Plant Biol 58:44–51

    Article  CAS  Google Scholar 

  • Chen L, Auh C, Chen F, Cheng X, Aljoe H, Dixon RA, Wang Z (2002) Lignin deposition and associated changes in anatomy, enzyme activity, gene expression, and ruminal degradability in stems of tall fescue at different developmental stages. J Agric Food Chem 50:5558–5565

    Article  CAS  PubMed  Google Scholar 

  • Ching A, Dhugga KS, Appenzeller L, Meeley R, Bourett TM, Howard RJ, Rafalski A (2006) Brittle stalk 2 encodes a putative glycosylphosphatidylinositol-anchored protein that affects mechanical strength of maize tissues by altering the composition and structure of secondary cell walls. Planta 224:1174–1184

    Article  CAS  PubMed  Google Scholar 

  • Colburn MW, Evans JL (1967) Chemical composition of the cell-wall constituent and acid detergent fiber fractions of forages. J Dairy Sci 50:1130–1135

    Article  CAS  Google Scholar 

  • Collins M (1988) Composition and fibre digestion in morphological components of an alfalfa-timothy sward. Anim Feed Sci Tech 19:135–143

    Article  Google Scholar 

  • Emile JC, Gillet M, Ghesquière M, Charrier X (1992) Continuous grazing of tall fescue by dairy cows. Yield improvement by the use of a cultivar bred for a higher palatability. Fourrages 130:159–169 (In French)

    Google Scholar 

  • Fujimori M (2002) Breeding male-sterile tall fescue. Jpn Livestock Technol 562:15–18 (In Japanese)

    Google Scholar 

  • Grabber JH, Jung GA, Abrams SM, Howard DB (1992) Digestion kinetics of parenchyma and sclerenchyma cell walls isolated from orchardgrass and switchgrass. Crop Sci 32:806–810

    Article  CAS  Google Scholar 

  • Hirano K, Aya K, Morinaka Y, Nagamatsu S, Sato Y, Antonio BA, Namiki N, Nagamura Y, Matsuoka M (2013) Survey of genes involved in rice secondary cell wall formation through a co-expression network. Plant Cell Physiol 54:1803–1821

    Article  CAS  PubMed  Google Scholar 

  • Hiratsu K, Matsui K, Koyama T, Ohme-Takagi M (2003) Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis. Plant J 34:733–739

    Article  CAS  PubMed  Google Scholar 

  • Kokubo A, Sakurai N, Kuraishi S, Takeda K (1991) Culm brittleness of barley (Hordeum vulgare L.) mutants is caused by smaller number of cellulose molecules in cell wall. Plant Physiol 97:509–514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kubo M, Udagawa M, Nishikubo N, Horiguchi G, Yamaguchi M, Ito J, Mimura T, Fukuda H, Demura T (2005) Transcription switches for protoxylem and metaxylem vessel formation. Genes Dev 19:1855–1860

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Qian Q, Zhou Y, Yan M, Sun L, Zhang M, Fu Z, Wang Y, Han B, Pang X, Chen M, Li J (2003) BRITTLE CULM1, which encodes a COBRA-like protein, affects the mechanical properties of rice plants. Plant Cell 15:2020–2031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mertens DR, Ely LO (1979) A dynamic model of fiber digestion and passage in the ruminant for evaluating forage quality. J Anim Sci 49:1085–1095

    Article  Google Scholar 

  • Mitsuda N, Hiratsu K, Todaka D, Nakashima K, Yamaguchi-Shinozaki K, Ohme-Takagi M (2006) Efficient production of male and female sterile plants by expression of a chimeric repressor in Arabidopsis and rice. Plant Biotech J 4:325–332

    Article  CAS  Google Scholar 

  • Mitsuda N, Iwase A, Yamamoto H, Yoshida M, Seki M, Shinozaki K, Ohme-Takagi M (2007) NAC transcription factors, NST1 and NST3, are key regulators of the formation of secondary walls in woody tissues of Arabidopsis. Plant Cell 19:270–280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mitsuda N, Seki M, Shinozaki K, Ohme-Takagi M (2005) The NAC transcription factors NST1 and NST2 of Arabidopsis regulate secondary wall thickenings and are required for anther dehiscence. Plant Cell 17:2993–3006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oba M, Allen MS (1999) Evaluation of the importance of the digestibility of neutral detergent fiber from forage: effects on dry matter intake and milk yield of dairy cows. J Dairy Sci 82:589–596

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto S, Mitsuda N (2015) Reconstitution of a secondary cell wall in a secondary cell wall-deficient Arabidopsis mutant. Plant Cell Physiol 56:299–310

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto S, Takata N, Oshima Y, Yoshida K, Taniguchi T, Mitsuda N (2016) Wood reinforcement of poplar by rice NAC transcription factor. Sci Rep 6:19925

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sato H, Takamizo T (2006) Agrobacterium tumefaciens-mediated transformation of forage-type perennial ryegrass (Lolium perenne L.) Grassl Sci 52:95–98

    Article  CAS  Google Scholar 

  • Sato H, Yoshida K, Mitsuda N, Ohme-Takagi M, Takamizo T (2012) Male-sterile and cleistogamous phenotypes in tall fescue induced by chimeric repressors of SUPERWOMAN1 and OsMADS58. Plant Sci 183:183–189

    Article  CAS  PubMed  Google Scholar 

  • Simmons BA, Loque D, Blanch HW (2008) Next-generation biomass feedstocks for biofuel production. Genome Biol 9:242–247

    Article  PubMed  PubMed Central  Google Scholar 

  • Sindhu A, Langewisch T, Olek A, Multani DS, McCann MC, Vermerris W, Carpita NC, Johal G (2007) Maize Brittle stalk2 encodes a COBRA-like protein expressed in early organ development but required for tissue flexibility at maturity. Plant Physiol 145:1444–1459

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stone JB, Trimberger GW, Henderson CR, Reid JT, Turk KL, Loosli JK (1960) Forage intake and efficiency of feed utilization in dairy cattle. J Dairy Sci 43:1275–1281

    Article  Google Scholar 

  • Van Soest PJ (1963) Use of detergents in the analysis of fibrous feeds. II. A rapid method for the determination of fiber and lignin. J Assoc Off Anal Chem 46:829–835

    Google Scholar 

  • Wardrop AB (1971) Occurrence and formation in plants. In: Sarkanen KV, Ludwig CH (eds) Lignins: occurrence, formation structure and reactions. Wiley-Interscience, New York, pp 19–41

    Google Scholar 

  • Yang F, Mitra P, Zhang L, Prak L, Verhertbruggen Y, Kim J-S, Sun L, Zheng K, Tang K, Auer M, Scheller HV, Loque D (2013) Engineering secondary cell wall deposition in plants. Plant Biotecnol J 11:325–335

    Article  CAS  Google Scholar 

  • Yoshida K, Sakamoto S, Kawai T, Kobayashi Y, Sato K, Ichinose Y, Yaoi K, Akiyoshi-Endo M, Sato H, Takamizo T, Ohme-Takagi M, Mitsuda N (2013) Engineering the Oryza sativa cell wall with rice NAC transcription factors regulating secondary wall formation. Front Plant Sci 4:383–389

    Article  PubMed  PubMed Central  Google Scholar 

  • Yuan JS, Tiller KH, Al-Ahmad H, Stewart NR, Stewart Jr CN (2008) Plants to power: bioenergy to fuel the future. Trends Plant Sci 13:421–429

    Article  CAS  PubMed  Google Scholar 

  • Zhang K, Qian Q, Huang Z, Wang Y, Li M, Hong L, Zeng D, Gu M, Chu C, Cheng Z (2006) GOLD HULL AND INTERNODE2 encodes a primarily multifunctional cinnamyl-alcohol dehydrogenase in rice. Plant Physiol 140:972–983

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhong R, Demura T, Ye Z-H (2006) SND1, a NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of Arabidopsis. Plant Cell 18:3158–3170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhong R, Lee C, McCarthy RL, Reeves CK, Jones EG, Ye Z-H (2011) Transcriptional activation of secondary wall biosynthesis by rice and maize NAC and MYB transcription factors. Plant Cell Physiol 52:1856–1871

    Article  CAS  PubMed  Google Scholar 

  • Zhong R, Richardson EA, Ye Z-H (2007) Two NAC domain transcription factors, SND1 and NST1, function redundantly in regulation of secondary wall synthesis in fibers of Arabidopsis. Planta 225:1603–1611

    Article  CAS  PubMed  Google Scholar 

  • Zhong R, Ye Z-H (2014) Complexity of the transcriptional network controlling secondary wall biosynthesis. Plant Sci 229:193–207

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Ms. Aeni Hosaka, Ms. Kaori Mogi, Ms. Miyuki Sato, and Ms. Hitomi Takaishi for technical assistance. This work was supported by the Research and Development Program for New Bio-industry Initiatives from the Bio-oriented Technology Research Advancement Institution of Japan and the Advanced Low Carbon Technology Research and Development Program (ALCA) from Japan Science and Technology Agency (JST).

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Correspondence to Hiroko Sato.

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Supplemental Table 1

Primers used in this study. (GIF 81 kb)

High resolution image (TIFF 2933 kb)

Supplemental Table 2

Phenotypes of transgenic plants expressing OsSWN2-SRDX. *Number of transgenic plants that showed the phenotype/number of transgenic plants expressing OsSWN2-SRDX. (GIF 76 kb)

High resolution image (TIFF 2933 kb)

Supplemental Fig. 1

Phenotypes of the transgenic and non-transgenic plants at flowering stage. a Wild-type plant (N1). b OsSWN2-SRDX plant (no. 4). c OsSWN2-SRDX plant (no. 2). Arrows indicate drooping stems. (GIF 177 kb)

High resolution image (TIFF 2933 kb)

Supplemental Fig. 2

AIR/FW of the transgenic plants and non-transgenic plants. a The ratio of AIR/FW in stems. b The ratio of AIR/FW in leaves. Error bars represent SD of quadruplicate experiments. *Significantly different from each source plant by Dunnett’s test at P < 0.05. (GIF 202 kb)

High resolution image (TIFF 5210 kb)

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Sato, H., Sakamoto, S., Mitsuda, N. et al. Improvement of cell wall digestibility in tall fescue by Oryza sativa SECONDARY WALL NAC DOMAIN PROTEIN2 chimeric repressor. Mol Breeding 38, 36 (2018). https://doi.org/10.1007/s11032-018-0796-z

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