Skip to main content
SpringerLink
Log in

Occurrence and tolerance mechanisms of seed cracking under low temperatures in soybean (Glycine max)

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

In soybean, occurrence of, or tolerance to, seed cracking under low temperatures may be related to the presence or absence, respectively, of proanthocyanidin accumulation in the seed coat dorsal region.

Soybean seeds sometimes undergo cracking during low temperatures in summer. In this study, we focused on the occurrence and tolerance mechanisms of low-temperature-induced seed cracking in the sensitive yellow soybean cultivar Yukihomare and the tolerant yellow soybean breeding line Toiku 248. Yukihomare exhibited seed cracking when subjected to a 21-day low-temperature treatment from 10 days after flowering. In yellow soybeans, seed coat pigmentation is inhibited, leading to low proanthocyanidin levels in the seed coat. Proanthocyanidins accumulated on the dorsal side of the seed coat in Yukihomare under the 21-day low-temperature treatment. In addition, a straight seed coat split occurred on the dorsal side at the full-sized seed stage, resulting in seed cracking in this cultivar. Conversely, proanthocyanidin accumulation was suppressed throughout the seed coat in low-temperature-treated Toiku 248. We propose the following mechanism of seed cracking: proanthocyanidin accumulation and subsequent lignin deposition under low temperatures affects the physical properties of the seed coat, making it more prone to splitting. Further analyses uncovered differences in the physical properties of the seed coat between Yukihomare and Toiku 248. In particular, seed coat hardness decreased in Yukihomare, but not in Toiku 248, under the low-temperature treatment. Seed coat flexibility was higher in Toiku 248 than in Yukihomare under the low-temperature treatment, suggesting that the seed coat of low-temperature-treated Toiku 248 is more flexible than that of low-temperature-treated Yukihomare. These physical properties of the Toiku 248 seed coat observed under low-temperature conditions may contribute to its seed-cracking tolerance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

Abbreviations

CD:

Cold-induced seed coat discoloration

CHS:

Chalcone synthase

DMACA:

4-Dimethylaminocinnamaldehyde

dNS:

Developing non-SC seeds

dSS:

Developing SC seeds

PA:

Proanthocyanidin

QTL:

Quantitative trait locus

SC:

Seed cracking

THM:

Seed coat pigmented mutant of cv. Toyohomare

T248:

Breeding line Toiku 248

YH:

cv. Yukihomare

References

  • Barros J, Serk H, Granlund I, Pesquet E (2015) The cell biology of lignification in higher plants. Ann Bot 115:1053–1074

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bernard RL, Weiss MG (1973) Qualitative genetics. In: Caldwell BE (ed) Soybean: Improvement, production, and uses. American Society of Agronomy, Madison, pp 117–154

    Google Scholar 

  • Delessert C, Wilson I, Van Der Straeten D, Dennis E, Dolferus R (2004) Spatial and temporal expression of the local response to wounding. Plant Mol Biol 55:165–181

    Article  PubMed  CAS  Google Scholar 

  • Funatsuki H, Ohnishi S (2009) Recent advances in physiological and genetic studies on chilling tolerance in soybean. JARQ Jpn Agric Res Q 43:95–101

    Article  Google Scholar 

  • Kasai A, Kasai K, Yumoto S, Senda M (2007) Structural features of GmIRCHS, candidate of the I gene inhibiting seed coat pigmentation in soybean: implications for inducing endogenous RNA silencing of chalcone synthase genes. Plant Mol Biol 64:467–479

    Article  PubMed  CAS  Google Scholar 

  • Kasai A, Ohnishi S, Yamazaki H, Funatsuki H, Kurauchi T, Matsumoto T, Yumoto S, Senda M (2009) Molecular mechanism of seed coat discoloration induced by low temperature in yellow soybean. Plant Cell Physiol 50:1090–1098

    Article  PubMed  CAS  Google Scholar 

  • Kim YJ, Kim DG, Lee SH, Lee I (2006) Wound-induced expression of the ferulate 5-hydroxylase gene in Camptotheca acuminata. Biochim Biophys Acta 1760:182–190

    Article  PubMed  CAS  Google Scholar 

  • Kurauchi T, Kasai A, Tougou M, Senda M (2011) Endogenous RNA interference of chalcone synthase genes in soybean: formation of double-stranded RNA of GmIRCHS transcripts and structure of the 5′ and 3′ ends of short interfering RNAs. J Plant Physiol 168:1264–1270

    Article  PubMed  CAS  Google Scholar 

  • Liang M, Davis E, Gardner D, Cai X, Wu Y (2006) Involvement of AtLAC15 in lignin synthesis in seeds and in root elongation of Arabidopsis. Planta 224:1185–1196

    Article  PubMed  CAS  Google Scholar 

  • Liu HL (1949) Inheritance of defective seed coat in soybeans. J Hered 40:317–322

    Article  Google Scholar 

  • Morrison MJ, Pietrzak LN, Voldeng HD (1998) Soybean seed coat discoloration in cool-season climates. Agron J 90:471–474

    Article  Google Scholar 

  • Nicholas CD, Lindstrom JT, Vodkin LO (1993) Variation of proline rich cell wall proteins in soybean lines with anthocyanin mutations. Plant Mol Biol 21:145–156

    Article  PubMed  CAS  Google Scholar 

  • Ohnishi S, Funatsuki H, Kasai A, Kurauchi T, Yamaguchi N, Takeuchi T, Yamazaki H, Kurosaki H, Shirai S, Miyoshi T, Horita H, Senda M (2011) Variation of GmIRCHS (Glycine max inverted-repeat CHS pseudogene) is related to tolerance of low temperature-induced seed discoloration in yellow soybean. Theor Appl Genet 122:633–642

    Article  PubMed  Google Scholar 

  • Percy JD, Philip R, Vodkin LO (1999) A defective seed coat pattern (Net) is correlated with the post-transcriptional abundance of soluble proline-rich cell wall proteins. Plant Mol Biol 40:603–613

    Article  PubMed  CAS  Google Scholar 

  • Qutob D, Ma F, Peterson CA, Bernards MA, Gijzen M (2008) Structural and permeability properties of the soybean seed coat. Botany 86:219–227

    Article  Google Scholar 

  • Ritchie SW, Hanway JJ, Thompson HE, Benson GO (1985) How a soybean plant develops. Special Report No. 53. Iowa State University of Science and Technology Cooperative Extension Service, Ames

    Google Scholar 

  • Senda M, Masuta C, Ohnishi S, Goto K, Kasai A, Sano T, Hong JS, MacFarlane S (2004) Patterning of virus-infected Glycine max seed coat is associated with suppression of endogenous silencing of chalcone synthase genes. Plant Cell 16:807–818

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Senda M, Kurauchi T, Kasai A, Ohnishi S (2012) Suppressive mechanism of seed coat pigmentation in yellow soybean. Breed Sci 61:523–530

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Senda M, Yamaguchi N, Hiraoka M, Kawada S, Iiyoshi R, Yamashita K, Sonoki T, Maeda H, Kawasaki M (2017) Accumulation of proanthocyanidins and/or lignin deposition in buff-pigmented soybean seed coats may lead to frequent defective cracking. Planta 245:659–670

    Article  PubMed  CAS  Google Scholar 

  • Shaipulah NFM, Muhlemann JK, Woodworth BD, Moerkercke AV, Verdonk JC, Ramirez AA, Haring MA, Dudareva N, Shuurink RC (2016) CCoAOMT down-regulation activates anthocyanin biosynthesis in petunia. Plant Physiol 170:717–731

    Article  PubMed  CAS  Google Scholar 

  • Soltani BM, Ehlting J, Hamberger B, Douglas CJ (2006) Multiple cis-regulatory elements regulate distinct and complex patterns of developmental and wound-induced expression of Arabidopsis thaliana 4CL gene family members. Planta 224:1226–1238

    Article  PubMed  CAS  Google Scholar 

  • Srinivasan A, Arihara J (1994) Soybean seed discoloration and cracking in response to low temperatures during early reproductive growth. Crop Sci 34:1611–1617

    Article  Google Scholar 

  • Stewart RT, Wentz JB (1930) A defective seed-coat character in soybeans. J Am Soc Agron 22:658–662

    Article  Google Scholar 

  • Szittya G, Silhavy D, Molnár A, Havelda Z, Lovas Á, Lakatos L, Bánfalvi Z, Burgyán J (2003) Low temperature inhibits RNA silencing-mediated defence by the control of siRNA generation. EMBO J 22:633–640

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Takahashi R, Abe J (1994) Genetic and linkage analysis of low temperature-induced browning in soybean seed coats. J Hered 85:447–450

    Article  Google Scholar 

  • Takahashi R, Abe J (1999) Soybean maturity genes associated with seed coat pigmentation and cracking in response to low temperatures. Crop Sci 39:1657–1662

    Article  Google Scholar 

  • Todd JJ, Vodkin LO (1993) Pigmented soybean (Glycine max) seed coats accumulate proanthocyanidins during development. Plant Physiol 102:663–670

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tuteja JH, Clough SJ, Chan W-C, Vodkin LO (2004) Tissue-specific gene silencing mediated by a naturally occurring chalcone synthase gene cluster in Glycine max. Plant Cell 16:819–835

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yamaguchi N, Yamazaki H, Ohnishi S, Suzuki C, Hagihara S, Miyoshi T, Senda M (2014) Method for selection of soybeans tolerant to seed cracking under chilling temperatures. Breed Sci 64:103–108

    Article  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi N, Taguchi-Shiobara F, Sayama T, Miyoshi T, Kawasaki M, Ishimoto M, Senda M (2015) Quantitative trait loci associated with tolerance to seed cracking under chilling temperature in soybean. Crop Sci 55:2100–2107

    Article  CAS  Google Scholar 

  • Zabala G, Vodkin L (2003) Cloning of the pleiotropic T locus in soybean and two recessive alleles that differentially affect structure and expression of the encoded flavonoid 3′ hydroxylase. Genetics 163:295–309

    PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Ministry of Agriculture, Forestry, and Fisheries of Japan [Genomics-based Technology for Agricultural Improvement, SFC1006 (to MS, MK, HM, and NY)] and the Japan Society for the Promotion of Science [KAKENHI, grant number 15K07268 (to MS)]. We thank Jennifer Smith, PhD, Emma Tacken, Ph.D., and Barbara Goodson, PhD from Edanz Group (http://www.edanzediting.com/ac) for editing a draft of this manuscript.

Author information

Authors and Affiliations

  1. Faculty of Agriculture and Life Science, Hirosaki University, 3 Bunkyo, Hirosaki, Aomori, 036-8561, Japan

    Mineo Senda, Michio Kawasaki, Miho Hiraoka, Kazuki Yamashita & Hayato Maeda

  2. Hokkaido Research Organization, Tokachi Agricultural Experiment Station, Shinsei, Memuro-cho, Kasai-gun, Hokkaido, 082-0081, Japan

    Naoya Yamaguchi

Authors
  1. Mineo Senda
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michio Kawasaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Miho Hiraoka
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kazuki Yamashita
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hayato Maeda
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Naoya Yamaguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mineo Senda.

Ethics declarations

Conflict of interest

Authors declare that they have no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplemental Fig. S1

Cross sections of seed coats of YH and T248 grown under normal conditions (YH-N and T248-N, respectively). Seed coat sections were stained with DMACA to show PA accumulation. a YH-N (hilum region), b YH-N (middle region), c YH-N (dorsal region), d T248-N (hilum region), e T248-N (middle region), f T248-N (dorsal region). Hilum, middle, and dorsal regions are shown in Fig. 2e. pa, parenchyma; pl, palisade layer; tb, tracheid bar. Scale bars 100 μm (a, d) and 20 μm (b, c, e, f) (PPTX 11174 kb)

Supplemental Fig. S2

Comparison of seed coat physical properties among YH-N, YH-L dNS, and YH-L dSS. Vertical bars represent mean ± SD [n = 51 for YH-N, n = 29 for YH-L (dNS), and n = 22 for YH-L (dSS)]. Different letters indicate significant differences at P < 0.05 by Tukey–Kramer’s test (PPTX 43 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Senda, M., Kawasaki, M., Hiraoka, M. et al. Occurrence and tolerance mechanisms of seed cracking under low temperatures in soybean (Glycine max). Planta 248, 369–379 (2018). https://doi.org/10.1007/s00425-018-2912-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-018-2912-z

Keywords

Search

Navigation