Mechanisms regulating the boron nutritional status in rapeseed and Arabidopsis and their implications for the development of boron-efficient genotypes
Final Report Abstract
Boron (B) is an essential micronutrient for seed plants. Although numerous effects of nutritional B imbalances on the growth and the physiology of plants have been described, the genetic and molecular basics for mechanisms sensing and regulating the nutritional B status as well as B efficiency mechanisms and the B functions themselves are mostly unknown. It still holds true, that the role of B in plant physiology is the least understood of all the mineral plant nutrients. This is surprising, as B is one of the most frequently deficient and actively managed micronutrients in crops and B fertilization is critical for achieving optimal agricultural productivity. B-limiting conditions have detrimental consequences for crop plant fertility and for root performance, as B deficiency inhibits root growth and root functions almost immediately. Therefore, the main objectives of this Emmy Noether group were to elucidate B efficiency traits, biochemical functions, transport pathways and regulatory networks of B in plants, as well as their transcriptional, developmental and signalling responses to B deficiency and toxicity. To this aim, the Emmy Noether group synergistically bridged classic plant nutritional research with modern molecular biology, and extensively exploited the genetic diversity for B efficiency traits in Arabidopsis thaliana accessions as well as in Brassica napus cultivars deriving from the Genebank of the Leibniz Institute of Plant Genetics and Crop Plant Research (IPK) in Gatersleben, inter alia in the modern IPK shoot and root phenotyping facilities. On top of that, a combination of detailed physiological measurements, genetic approaches, elemental analyses, transcriptomic and metabolomic profiling, transport studies and targeted molecular analyses were performed on plants and using the Saccharomyces cerevisiae and Xenopus laevis heterologous expression systems, in order to genetically identify and molecularly and physiologically characterise mechanisms regulating the B nutritional status in B. napus and Arabidopsis. Scientific key achievements of this Emmy Noether project are: • Establishment of a unique soil substrate^ased cultivation system which is suitable to study and quantify shootC and root traits of plants being cultivated under highly controlled and repeatable B nutrient supply regimes, also in automated highCthroughput phenotyping facilities. Such a system is unique so far. • ScreeningCbased identification of a few highly BCefficient Arabidopsis (amongst ~188 accessions) and B. napus (amongst ~590 cultivars) genotypes which are currently serving as valuable resources to identify and study genetic, molecular and physiological factors which determine B efficiency in plants. • Generation of a doubled haploid (DH) B. napus population which was created from a cross of identified IPK Genebank genotypes contrasting in their B efficiency and in their root system architecture. • ChipCgenotyping & spatiotemporal root/shoot imagingCbased, elemental and physical phenotyping of the B. napus DH population grown under defined BCsufficient and BCdeficient soi^substrate growth conditions. • Identification of shoot/root B efficiencyCresponsible candidate genes in B. napus and Arabidopsis by QTL and GWAS analyses, and ongoing characterization by RNACsequencing and reverse genetic analyses. • Evidence has been obtained that the B transport protein (Nodulin26Clike Intrinsic Proteins (NIPs) and BORs) Cmediated uptake and translocation ability, root system architecture traits and phytohormone signalling are key factors contributing to B deficiency tolerance. • Identification of molecular NIP protein characteristics which contribute to metalloid transport selectivity in plants. These findings may contribute to the generation of plants which possess efficient B transport pathways without increasing the transport of the toxic mineral arsenic (As) to edible plant parts. • Uncovering of the functional evolution of plant NIP channel proteins along the phylogenetic tree of green plants and the demonstration that evolution has turned crucial bacterial As efflux transporters, after their horizontal gene transfer, into essential B and Si NIP importers in seed plants. • Identification and molecular characterization of numerous NIP channel proteins from B. napus. This information allows understanding the uptake and translocation processes of metalloids at the cellular level in more detail. Moreover, novel NIP channel features and characteristics were identified. The obtained data significantly advanced the knowledge on this channel protein family. In summary, the findings of the Emmy Noether project have provided a variety of new aspects and novel insights into the mechanisms regulating the B nutritional status in plants. Based on the generated knowledge, the established methods and the developed resources, followup studies will further reveal B efficiency mechanisms and their underlying genes. The obtained knowledge will help to understand plant responses to B deficiency, assist to develop BCefficient genotypes and contribute to an intelligent B fertilization management in the field, which will contribute to a more sustainable agriculture in future.
Publications
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(2015) Genome-wide identification of aquaporin encoding genes in Brassica oleracea and their phylogenetic sequence comparison to Brassica crops and Arabidopsis. Frontiers in Plant Science 6: 166
Diehn TA, Pommerrenig B, Bernhardt N, Hartmann A, Bienert GP
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(2016) Pollen-specific aquaporins NIP4;1 and NIP4;2 are required for pollen development and pollination in Arabidopsis thaliana. The Plant Cell 28: 1053-1077
Pérez Di Giorgio JA, Bienert GP, Ayub ND, Yaneff A, Barberini ML, Mecchia MA, Amodeo G, Soto GS, Muschietti JP
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(2018) Heterotetramerization of plant PIP1 and PIP2 aquaporins is an evolutionary ancient feature to control channel trafficking and functionality. Frontiers in Plant Science 9: 382
Bienert MD, Diehn TA, Richet N, Chaumont F, Bienert GP
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(2018) Identification of rapeseed (Brassica napus) cultivars with a high tolerance to boron deficient conditions. Frontiers in Plant Science 9: 1142
Pommerrenig B, Junker A, Sanchez Abreu I, Bieber A, Fuge J, Willner E, Bienert MD, Altmann T, Bienert GP
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(2019) Boron deficiency effects on sugar, ionome, and phytohormone profiles of vascular and non-vascular leaf tissues of common plantain (Plantago major). International Journal of Molecular Sciences 20: 3882
Pommerrenig B, Eggert K, Bienert GP
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(2019) Boron demanding tissues of Brassica napus express specific sets of functional Nodulin26-like Intrinsic Proteins and BOR1 transporters. Plant Journal 100: 68-82
Diehn TA, Bienert MD, Pommerrenig B, Liu Z, Spitzer C, Bernhardt N, Fuge J, Bieber A, Richet N, Chaumont F, Bienert GP
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(2019) Boron: an essential element for vascular plants. New Phytologist
Wimmer M, Abreu I, Bell R, Bienert MD, Brown P, Dell B, Fujiwara T, Goldbach H, Lehto T, Mock HP, von Wirén N, Bassil E, Bienert GP
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(2019) Overexpression of X Intrinsic Protein 1;1 in Nicotiana tabacum and Arabidopsis reduces boron allocation to shoot sink tissues. Plant Direct 3: e00143
Bienert MD, Muries B, Crappe D, Chaumont F, Bienert GP
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(2019) Root system size response of bzh semi-dwarf oilseed rape hybrids to different nitrogen levels in the field. Annals of Botany 124: 883890
Schierholt A, Tietz T, Bienert GP, Gertz A, Miersch S, Becker H
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(2020) Functional evolution of Nodulin26-like Intrinsic Proteins: From bacterial arsenic detoxification to plant nutrient transport. New Phytologist 225: 1383-1396
Pommerrenig B, Diehn TA, Bernhardt N, Bienert MD, Mitani N, Fuge J, Bieber A, Spitzer C, Bräutigam A, Ma JF, Chaumont F, Bienert GP
