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Cotyledons contribute to plant growth and hybrid vigor in Arabidopsis

  • Li Wang
  • Pei-Chuan Liu
  • Li Min Wu
  • Jiafu Tan
  • W. James Peacock
  • Elizabeth S. Dennis
Original Article
  • 144 Downloads

Abstract

Main conclusion

In hybrids of Arabidopsis, cotyledons influence the amount and proportion of hybrid vigor in total plant growth.

We found Arabidopsis cotyledons are essential for plant growth and in some hybrids for hybrid vigor. In hybrids between C24 and Landsberg erecta (Ler), biomass vigor (heterosis) occurs in the first few days after sowing (DAS), with hybrid cotyledons being larger than those of their parents. C24xLer hybrids are ahead of their parents in activating photosynthesis and auxin pathway genes in cotyledons at 3–4 DAS. “Earliness” is also present in newly emerged C24xLer hybrid leaves. We showed cotyledon removal at 4 DAS caused significant biomass reduction in later growth in hybrids and parental lines. The biomass decrease caused by cotyledon removal can be partially rescued by exogenous sucrose or auxin with different genotypes responding to sucrose and/or auxin differently. Cotyledon removal has different effects on heterosis in different hybrids. After cotyledon removal, in C24xLer hybrids, both growth and heterosis were reduced in similar proportions, but the level of hybrid vigor was reduced as a proportion of growth in C24xColumbia (Col) and ColxLer hybrids. The removal of cotyledons at 4 DAS markedly decreased the level of growth and eliminated the heterotic phenotype of Wassilewskija (Ws)/Ler hybrids. In mutant Ws/Ler hybrids which had a reduced level of photosynthesis in the cotyledons, there was a reduction in plant growth and loss of heterosis. The variation in contribution of cotyledons to heterosis in different hybrids indicates there are multiple pathways to achieve heterotic phenotypes.

Keywords

Auxin Heterosis Photosynthesis PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) Shi-yo-u 1 (cyo1Snowy cotyledon 2 (sco2) 

Abbreviations

cyo1

Shi-yo-u 1

DAS

Day after sowing

FW

Fresh weight

IAA29

INDOLE-3-ACETIC ACID INDUCIBLE 29

LHCB2.3

LIGHT-HARVESTING CHLOROPHYLL B-BINDING 2

MPV

Mid-parent value

NAA

1-Naphthaleneacetic acid

PIF4

PHYTOCHROME-INTERACTING FACTOR 4

PSAO

PHOTOSYSTEM I SUBUNIT O

sco1

Snowy cotyledon 1

YUC8

YUCCA8

Notes

Acknowledgements

We thank Dr. Ken-ichiro Takamiya in Tokyo Institute of Technology and Professor Barry Pogson at the Australia National University for providing cyo1 and sco2 mutant seeds, Aihua Wang and Bjorg Sherman for technical assistance, Neil Smith, Dr. Ian Greaves and Dr. Anyu Zhu for helpful discussion and suggestions on this project, Dr. Ming-Bo Wang, Dr. Masumi Robertson and Dr. TJ Higgins for manuscript reviewing.

Compliance with ethical standards

Conflict of interest

The authors declare no competing interests.

Supplementary material

425_2018_3068_MOESM1_ESM.xlsx (26 kb)
Supplementary material 1 (XLSX 26 kb)
425_2018_3068_MOESM2_ESM.pdf (902 kb)
Fig. S1 Cotyledon removal at 7 or 10 DAS had less effect on plant biomass at 15 DAS than removal at 4 DAS. The phenotypes (a) and FWs (b) of 15-day-old parents (C24 and Ler), and two reciprocal hybrids (C24xLer and LerxC24) with cotyledon removed (-Cot) at 4, 7 and 10 DAS. The intact parents and hybrid plants are used as controls (Control). n > 10. Scale bar = 1 cm applies to all images. *indicates significant differences from the MPV at P (Student’s t test) < 0.05. Error bars = SE. Fig. S2 Plants with cotyledon removed had a slower developmental rate than the intact plants. a The flowering time of the parents and hybrids having cotyledons removed (-Cot) at 4 DAS compared to the control plants. b The number of rosette leaves produced at the time of flowering in Ler and Ler having cotyledon removed at 4 DAS. * indicates significant differences at P (Student’s t test) < 0.05 from the control plants. Error bars = SE. n = 15 – 20. Fig. S3 The phenotypes of 15-day-old parents C24 and Ler and hybrids C24xLer growing on media with added sucrose or auxin compared to plants growing on standard media. “Control” indicates intact plants, “-Cot” indicates the plants had cotyledons removed at 4 DAS. Scale bar = 1 cm. Fig. S4 Cotyledon removal at 4 DAS caused biomass loss in a number of hybrid combinations. a Result of cotyledon removal experiment in Fig. 5a (EXP1_May2018) was confirmed in an independent sowing (EXP2_June2018). n = 9-18 per line. b A summary of the level of heterosis in two experiments. The numbers above columns indicate the level of heterosis in the hybrids with/without cotyledons removed. c The FWs of the parents Ws and Ler, and Ws/Ler hybrids with cotyledons removed (-Cot) at 4 DAS compared to the control plants at 19 DAS. * indicates significant differences at P (Student’s t test) < 0.05 from MPV. Error bars = SE. Fig. S5 cyo1 showed phenotypic variation in the colour of cotyledons (lL.G., light green; P, pale; W, white). Photo was taken at 10 DAS. Scale bar = 1 cm. Fig. S6 Loss of heterosis in cyo1/sco2 hybrid at 19 DAS. a The FWs of Ws, Ler, Ws/Ler hybrids, cyo1, sco2 and cyo1/sco2 hybrids at 19 DAS. Mutants were grouped by phenotype category. ** indicates significant differences at P (Student’s t test) < 0.01 from the MPV. Error bars = SE. b Photos of Ws, Ler, Ws/Ler hybrids, cyo1, sco2 and cyo1/sco2 hybrids at 19 DAS. Scale bar = 5 cm (PDF 902 kb)

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Li Wang
    • 1
  • Pei-Chuan Liu
    • 1
  • Li Min Wu
    • 2
  • Jiafu Tan
    • 1
  • W. James Peacock
    • 1
    • 2
  • Elizabeth S. Dennis
    • 1
    • 2
  1. 1.Faculty of ScienceUniversity of TechnologySydneyAustralia
  2. 2.Agriculture and Food, Commonwealth Scientific Industrial Research OrganisationCanberraAustralia

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