Why are silicas not metallic or metalloid



30.10.2019 16:07

Bacterial arsenic channel proteins are the precursors of efficient boron nutrient transporters in plants

IPK office Press and public relations
Leibniz Institute for Plant Genetics and Crop Plant Research

- “Nodulin26-like-intrinsic-proteins” (NIPs) are essential for the transport of the semimetals silicon and boron in plants. Their functional origin was previously unknown.
- An international collaboration of researchers has now discovered that plant NIPs are derived from a bacterial arsenic channel protein that entered plants through horizontal gene transfer.
- Bacterial AqpN genes, the precursors of plant silicon and boron transport proteins, are and were probably involved in the bacterial arsenic detoxification machinery. In the course of the evolution of modern seed plants, there was a change in function, the transport of essential and beneficial semi-metals.

Short roots, brittle branches, poor fertility - these are some of the symptoms that can occur as a result of boron deficiency in plants. Thanks to the transport proteins "Nodulin26-like-intrinsic-proteins" (NIPs), seed plants can efficiently absorb and distribute this essential micronutrient. However, plants have not always had this possibility. An international collaboration of researchers has now revealed that the evolutionary origin of NIPs lies in genetically encoded arsenic detoxification units in bacteria. With the help of horizontal gene transfer, a gene that plays an important role in the arsenic detoxification of bacteria was integrated into the genome of land plants. In the course of evolution, this gene changed for the further benefit of plants and now codes for proteins that have the semimetallic nutrient function transport capabilities of NIPs in higher plants.

The majority of essential micronutrients in plants - such as copper, iron, and zinc - are metals. The two semimetals boron and silicon are vital or extremely beneficial for the development of seed plants. For many other organisms, from bacteria to humans, including the lower plants, these semimetals are less important. Both "micronutrients" contribute to the correct formation and elasticity of cell walls in vascular plants and support the defense against pathogens and general stress tolerance. Another common property of these semimetals is that they are taken up in seed plants, which include all of our most important staple food producing crops, with the help of nodulin26-like-intrinsic channel proteins (NIPs) and distributed within the plant. NIPs are highly conserved proteins and are found in plants but not in other eukaryotes. They belong to the channel protein superfamily of aquaporins, which transport uncharged molecules such as water, hydrogen peroxide, glycerine, ammonia and semi-metals. Until recently, the origin of the transport selectivity of plant NIPs and their original functions were unknown.

By combining sequence analyzes, phylogenetic and genetic analyzes, an international group of researchers has now succeeded in uncovering the evolutionary-functional origin of plant NIPs. Under the direction of Dr. Gerd Patrick Bienert from the Emmy Noether research group “Metalloid Transport” at the Leibniz Institute for Plant Genetics and Crop Plant Research (IPK) in Gatersleben, the researchers showed that the protein group of plant NIPs was formed from a bacterial arsenic-transporting AqpN aquaporin after this was transferred into the genome by a horizontal gene transfer of a presumably charophytic alga.

The said bacterial ancestor of all plant NIPs was probably placed in an arsenic resistance operon and detoxified arsenic acid through efficient export out of the bacteria.
Like boron and silicon, arsenic is a semimetal. If you compare boric acid, silicic acid and arsenic acid, the semi-metal species transported by aquaporins, you can see that they are very similar in terms of their physico-chemical and steric properties, which are essential for transport by an aquaporin.

The researchers succeeded in identifying NIPs in evolutionarily low plants such as algae, mosses and ferns, which are very similar to the original bacterial proteins at the level of their transport selection barriers. Interestingly, these original NIPs, as well as their bacterial ancestors, are almost impermeable to water and silicon, but transported arsenic and boron. With the help of a mutant analysis, the researchers showed that a change in the functional selectivity of NIPs had taken place during the evolution of the terrestrial plants. Transport proteins, which were originally bacterial arsenic outflow channels, have turned into essential uptake channels for important nutrients that we find in our modern seed plants. The results published by the researchers also explain why crops that have a high need for boron or silicon, such as rice, often contain very high levels of toxic arsenic when grown on arsenic-rich soils: the original bacterial channel property transporting arsenic is still inherent in today's crop NIPs. This leads to arsenic being inadvertently taken up by NIPs on arsenic-containing soils, while at the same time they perform their actual task, namely boron and silicon effectively and distributing them within the plant.

“Nevertheless, without the possession of an original bacterial arsenic detoxification channel, our modern crops would not be able to regulate efficient boron or silicon transport and agriculturally relevant crop yields would probably not even begin to be as high”, describes Dr. Bienert the importance of the knowledge. Boron deficiency in agriculture and horticulture leads to yield losses. This is one of the reasons why the researchers in the “Metalloid Transport” group will continue to investigate the mechanisms that regulate the boron diet in plants - with the aim of optimizing the use of boron in the field and providing plants with a improved boron breeding efficiency.

Explanatory legend for the figure:
Bacteria have arsenic resistance (ars) operons that regulate the detoxification and export of arsenic (As). Some bacteria have an aqpN aquaporin gene in their ars operon, which facilitates the outflow of As (III) species. Arsenate [As (V)] gets into bacteria via phosphate transporters. The transcription of arsR is induced by As (V) and the subsequently formed protein ArsR in turn regulates the expression of aqpN and arsC. The chemical gradient required to ensure an As outflow through AqpNs is maintained by the catalytic reduction of As (V) to As (III) by the enzyme arsenate reductase (ArsC). An aqpN gene was likely transferred to charophytic algae by horizontal gene transfer. As a result, the so-called “Nodulin 26-like Intrinsic Proteins” (NIPs) developed from these AQPN-type channel proteins, which are essential for the uptake and translocation of the nutrients silicon (Si) and boron (B) in seed plants. The emergence of vascular plants went hand in hand with the increased need for the nutrients Si and B, as well as with structural changes in the NIP channel proteins, which led to the efficient regulation of B and Si transport.


Scientific contact:

Dr. Gerd Patrick Bienert
Leibniz Institute for Plant Genetics and Crop Plant Research (IPK) Gatersleben
Tel .: +49 39482 5385,
Email: [email protected]


Original publication:

Benjamin Pommerrenig et al. (2019), Functional evolution of Nodulin26 ‐ like Intrinsic Proteins: From bacterial arsenic detoxification to plant nutrient transport. New Phytologist. DOI: https://doi.org/10.1111/nph.16217


Additional Information:

http: // Figure (for free use):
https://ipk-cloud.ipk-gatersleben.de/s/jHi8kjZGKrbEfxZ


attachment
Jacqueline Fuge studies the effects of different semi-metals on the moss Physcomitrella patens.

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