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Article

Whether Gametophytes Are Reduced or Unreduced in Angiosperms Might Be Determined Metabolically

1
Plants, Soils, and Climate Department, Utah State University, Logan, UT 84322-4820, USA
2
Instituto Tecnológico de Santo Domingo, 10103 Santo Domingo, Dominican Republic
3
College of Pharmacy and Life Science, Jiujiang University, Jiujiang 332000, China
4
Sherwood Pet Health, Logan, UT 84321, USA
5
Caisson Laboratories, Inc., Smithfield, UT 84335, USA
6
Crop Improvement Division, Indian Grassland and Fodder Research Institute, 284003 Jhansi, India
7
Molecular Biology Program, University of Utah, Salt Lake City, UT 84112-5750, USA
8
Wescor, Inc. An Elitech Company, Logan, UT 84321, USA
9
Cytiva, Inc., Logan, UT 84321, USA
*
Author to whom correspondence should be addressed.
These authors contributed equally.
Genes 2020, 11(12), 1449; https://doi.org/10.3390/genes11121449
Received: 19 October 2020 / Revised: 23 November 2020 / Accepted: 27 November 2020 / Published: 2 December 2020
(This article belongs to the Special Issue Molecular Basis of Apomixis in Plants)
In angiosperms, meiotic failure coupled with the formation of genetically unreduced gametophytes in ovules (apomeiosis) constitute major components of gametophytic apomixis. These aberrant developmental events are generally thought to be caused by mutation. However, efforts to locate the responsible mutations have failed. Herein, we tested a fundamentally different hypothesis: apomeiosis is a polyphenism of meiosis, with meiosis and apomeiosis being maintained by different states of metabolic homeostasis. Microarray analyses of ovules and pistils were used to differentiate meiotic from apomeiotic processes in Boechera (Brassicaceae). Genes associated with translation, cell division, epigenetic silencing, flowering, and meiosis characterized sexual Boechera (meiotic). In contrast, genes associated with stress responses, abscisic acid signaling, reactive oxygen species production, and stress attenuation mechanisms characterized apomictic Boechera (apomeiotic). We next tested whether these metabolic differences regulate reproductive mode. Apomeiosis switched to meiosis when premeiotic ovules of apomicts were cultured on media that increased oxidative stress. These treatments included drought, starvation, and H2O2 applications. In contrast, meiosis switched to apomeiosis when premeiotic pistils of sexual plants were cultured on media that relieved oxidative stress. These treatments included antioxidants, glucose, abscisic acid, fluridone, and 5-azacytidine. High-frequency apomeiosis was initiated in all sexual species tested: Brassicaceae, Boechera stricta, Boechera exilis, and Arabidopsis thaliana; Fabaceae, Vigna unguiculata; Asteraceae, Antennaria dioica. Unreduced gametophytes formed from ameiotic female and male sporocytes, first division restitution dyads, and nucellar cells. These results are consistent with modes of reproduction and types of apomixis, in natural apomicts, being regulated metabolically. View Full-Text
Keywords: 5-azacytidine; abscisic acid; apomixis; apospory; diplospory; expression profiling; fluridone; metabolic homeostasis; oxidative stress; sucrose non-fermenting-related protein kinase 5-azacytidine; abscisic acid; apomixis; apospory; diplospory; expression profiling; fluridone; metabolic homeostasis; oxidative stress; sucrose non-fermenting-related protein kinase
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MDPI and ACS Style

Mateo de Arias, M.; Gao, L.; Sherwood, D.A.; Dwivedi, K.K.; Price, B.J.; Jamison, M.; Kowallis, B.M.; Carman, J.G. Whether Gametophytes Are Reduced or Unreduced in Angiosperms Might Be Determined Metabolically. Genes 2020, 11, 1449. https://doi.org/10.3390/genes11121449

AMA Style

Mateo de Arias M, Gao L, Sherwood DA, Dwivedi KK, Price BJ, Jamison M, Kowallis BM, Carman JG. Whether Gametophytes Are Reduced or Unreduced in Angiosperms Might Be Determined Metabolically. Genes. 2020; 11(12):1449. https://doi.org/10.3390/genes11121449

Chicago/Turabian Style

Mateo de Arias, Mayelyn, Lei Gao, David A. Sherwood, Krishna K. Dwivedi, Bo J. Price, Michelle Jamison, Becky M. Kowallis, and John G. Carman. 2020. "Whether Gametophytes Are Reduced or Unreduced in Angiosperms Might Be Determined Metabolically" Genes 11, no. 12: 1449. https://doi.org/10.3390/genes11121449

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