Determining the footprint of breeding in the seed microbiome of a perennial cereal

Kristina Michl; Christophe David; Benjamin Dumont; Linda-Maria Dimitrova Mårtensson; Frank Rasche; Gabriele Berg; Tomislav Cernava

doi:10.1186/s40793-024-00584-3

Determining the footprint of breeding in the seed microbiome of a perennial cereal

Environ Microbiome. 2024 Jun 17;19(1):40. doi: 10.1186/s40793-024-00584-3.

Authors

Kristina Michl¹, Christophe David², Benjamin Dumont³, Linda-Maria Dimitrova Mårtensson⁴, Frank Rasche^{5

6}, Gabriele Berg^{1

7

8}, Tomislav Cernava^{9

10}

Affiliations

¹ Institute of Environmental Biotechnology, Graz University of Technology, Graz, 8010, Austria.
² Department of Agroecosystems, Environment and Production, ISARA, 23 rue Jean Baldassini, Lyon Cedex 07, 69364, France.
³ Plant Sciences Axis, Crop Science lab, ULiege - Gembloux Agro-Bio Tech, Gembloux, B- 5030, Belgium.
⁴ Department of Biosystems and Technology, Swedish University of Agricultural Sciences, P.O. Box 103, Lomma, Alnarp, Sweden.
⁵ Institute of Agricultural Sciences in the Tropics (Hans-Ruthenberg-Institute), University of Hohenheim, 70593, Stuttgart, Germany.
⁶ International Institute of Tropical Agriculture, P.O. Box 30772-00100, Nairobi, Kenya.
⁷ Leibnitz-Institute for Agricultural Engineering, 14469, Potsdam, Germany.
⁸ Institute for Biochemistry and Biology, University of Potsdam, 14476, Potsdam, Germany.
⁹ Institute of Environmental Biotechnology, Graz University of Technology, Graz, 8010, Austria. tomislav.cernava@tugraz.at.
¹⁰ School of Biological Sciences, Faculty of Environmental and Life Sciences, University of Southampton, Southampton, SO171BJ, UK. tomislav.cernava@tugraz.at.

Abstract

Background: Seed endophytes have a significant impact on plant health and fitness. They can be inherited and passed on to the next plant generation. However, the impact of breeding on their composition in seeds is less understood. Here, we studied the indigenous seed microbiome of a recently domesticated perennial grain crop (Intermediate wheatgrass, Thinopyrum intermedium L.) that promises great potential for harnessing microorganisms to enhance crop performance by a multiphasic approach, including amplicon and strain libraries, as well as molecular and physiological assays.

Results: Intermediate wheatgrass seeds harvested from four field sites in Europe over three consecutive years were dominated by Proteobacteria (88%), followed by Firmicutes (10%). Pantoea was the most abundant genus and Pantoea agglomerans was identified as the only core taxon present in all samples. While bacterial diversity and species richness were similar across all accessions, the relative abundance varied especially in terms of low abundant and rare taxa. Seeds from four different breeding cycles (TLI C3, C5, C704, C801) showed significant differences in bacterial community composition and abundance. We found a decrease in the relative abundance of the functional genes nirK and nifH as well as a drop in bacterial diversity and richness. This was associated with a loss of amplicon sequence variants (ASVs) in Actinobacteria, Alphaproteobacteria, and Bacilli, which could be partially compensated in offspring seeds, which have been cultivated at a new site. Interestingly, only a subset assigned to potentially beneficial bacteria, e.g. Pantoea, Kosakonia, and Pseudomonas, was transmitted to the next plant generation or shared with offspring seeds.

Conclusion: Overall, this study advances our understanding of the assembly and transmission of endophytic seed microorganisms in perennial intermediate wheatgrass and highlights the importance of considering the plant microbiome in future breeding programs.

Keywords: Amplicon sequencing; Endophytes; Perennial grain; Plant breeding; Seed microbiome.