Magnesium (Mg2+) is an essential nutrient in all organisms. However, high levels of Mg2+ in the environment are toxic to plants. In this study, we identified the vacuolar-type H+-pyrophosphatase, AVP1, as a critical enzyme for optimal plant growth under high-Mg conditions. The Arabidopsis avp1 mutants displayed severe growth retardation, as compared to the wild-type plants upon excessive Mg2+. Unexpectedly, the avp1 mutant plants retained similar Mg content to wild-type plants under either normal or high Mg conditions, suggesting that AVP1 may not directly contribute to Mg2+ homeostasis in plant cells. Further analyses confirmed that the avp1 mutant plants contained a higher pyrophosphate (PPi) content than wild type, coupled with impaired vacuolar H+-pyrophosphatase activity. Interestingly, expression of the Saccharomyces cerevisiae cytosolic inorganic pyrophosphatase1 gene IPP1, which facilitates PPi hydrolysis but not proton translocation into vacuole, rescued the growth defects of avp1 mutants under high-Mg conditions. These results provide evidence that high-Mg sensitivity in avp1 mutants possibly resulted from elevated level of cytosolic PPi. Moreover, genetic analysis indicated that mutation of AVP1 was additive to the defects in mgt6 and cbl2 cbl3 mutants that are previously known to be impaired in Mg2+ homeostasis. Taken together, our results suggest AVP1 is required for cellular PPi homeostasis that in turn contributes to high-Mg tolerance in plant cells.
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The fluoride transporter FLUORIDE EXPORTER (FEX) is the major mechanism of tolerance to fluoride toxicity in plants1
Abstract Fluoride is everywhere in the environment, yet it is toxic to living things. How biological organisms detoxify fluoride has been unknown until recently. Fluoride-specific ion transporters in both prokaryotes (Fluoride channel; Fluc) and fungi (Fluoride Exporter; FEX) efficiently export fluoride to the extracellular environment. FEX homologs have been identified throughout the plant kingdom. Understanding the function of FEX in a multicellular organism will reveal valuable knowledge about reducing toxic effects caused by fluoride. Here, we demonstrate the conserved role of plant FEX (FLUORIDE EXPORTER) in conferring fluoride tolerance. Plant FEX facilitates the efflux of toxic fluoride ions from yeast cells and is required for fluoride tolerance in plants. A CRISPR/Cas9-generated mutation in Arabidopsis thaliana FEX renders the plant vulnerable to low concentrations (100-µM) of fluoride at every stage of development. Pollen is particularly affected, failing to develop even at extremely low levels of fluoride in the growth medium. The action of the FEX membrane transport protein is the major fluoride defense mechanism in plants.
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- Award ID(s):
- 1953903
- NSF-PAR ID:
- 10312929
- Date Published:
- Journal Name:
- Plant Physiology
- Volume:
- 186
- Issue:
- 2
- ISSN:
- 0032-0889
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract The rapid human‐driven changes in the environment during the Anthropocene have placed extreme stress on many plants and animals. Beneficial interactions with microorganisms may be crucial for ameliorating these stressors and facilitating the ecosystem services host organisms provide. Foliar endophytes, microorganisms that reside within leaves, are found in essentially all plants and can provide important benefits (e.g., enhanced drought tolerance or resistance to herbivory). However, it remains unclear how important the legacy effects of the abiotic stressors that select on these microbiomes are for affecting the degree of stress amelioration provided to their hosts. To elucidate foliar endophytes' role in host‐plant salt tolerance, especially if salinity experienced in the field selects for endophytes that are better suited to improve the salt tolerance of their hosts, we combined field collections of 90 endophyte communities from 30 sites across the coastal Everglades with a manipulative growth experiment assessing endophyte inoculation effects on host‐plant performance. Specifically, we grew >350 red mangrove (
Rhizophora mangle ) seedlings in a factorial design that manipulated the salinity environment the seedlings experienced (freshwater vs. saltwater), the introduction of field‐collected endophytes (live vs. sterilized inoculum), and the legacy of salinity stress experienced by these introduced endophytes, ranging from no salt stress (0 parts per thousand [ppt] salinity) to high salt stress (40 ppt) environments. We found that inoculation with field‐collected endophytes significantly increased mangrove performance across almost all metrics examined (15%–20% increase on average), and these beneficial effects typically occurred when the endophytes were grown in saltwater. Importantly, our study revealed the novel result that endophyte‐conferred salinity tolerance depended on microbiome salinity legacy in a key coastal foundation species. Salt‐stressed mangroves inoculated with endophyte microbiomes from high‐salinity environments performed, on average, as well as plants grown in low‐stress freshwater, while endophytes from freshwater environments did not relieve host salinity stress. Given the increasing salinity stress imposed by sea level rise and the importance of foundation species like mangroves for ecosystem services, our results indicate that consideration of endophytic associations and their salinity legacy may be critical for the successful restoration and management of coastal habitats. -
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Abstract Little is known about the tolerances of mammalian herbivores to plant specialized metabolites across landscapes.
We investigated the tolerances of two species of herbivorous woodrats,
Neotoma lepida (desert woodrat) andNeotoma bryanti (Bryant's woodrat) to creosote bushLarrea tridentata , a widely distributed shrub with a highly toxic resin. Woodrats were sampled from 13 locations both with and without creosote bush across a 900 km transect in the US southwest. We tested whether these woodrat populations consume creosote bush using plant metabarcoding of faeces and quantified their tolerance to creosote bush through feeding trials using chow amended with creosote resin.Toxin tolerance was analysed in the context of population structure across collection sites with microsatellite analyses. Genetic differentiation among woodrats collected from different locations was minimal within either species. Tolerance differed substantially between the two species, with
N. lepida persisting 20% longer thanN. bryanti in feeding trials with creosote resin. Furthermore, in both species, tolerance to creosote resin was similar among woodrats near or within creosote bush habitat. In both species, woodrats collected >25 km from creosote had markedly lower tolerances to creosote resin compared to animals from within the range of creosote bush.The results imply that mammalian herbivores are adapted to the specialized metabolites of plants in their diet, and that this tolerance can extend several kilometres outside of the range of dietary items. That is, direct ecological exposure to the specialized chemistry of particular plant species is not a prerequisite for tolerance to these compounds. These findings lay the groundwork for additional studies to investigate the genetic mechanisms underlying toxin tolerance and to identify how these mechanisms are maintained across landscape‐level scales in mammalian herbivores.
Read the free
Plain Language Summary for this article on the Journal blog. -
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Abstract Woody plant species store nonstructural carbohydrates (NSCs) for many functions. While known to buffer against fluctuations in photosynthetic supply, such as at night, NSC stores are also thought to buffer against environmental extremes, such as drought or freezing temperatures by serving as either back‐up energy reserves or osmolytes. However, a clear picture of how NSCs are shaped by climate is still lacking. Here, we update and leverage a unique global database of seasonal NSC storage measurements to examine whether maximum total NSC stores and the amount of soluble sugars are associated with clinal patterns in low temperatures or aridity, indicating they may confer a benefit under freezing or drought conditions. We examine patterns using the average climate at each study site and the unique climatic conditions at the time and place in which the sample was taken. Altogether, our results support the idea that NSC stores act as critical osmolytes. Soluble Sugars increase with both colder and drier conditions in aboveground tissues, indicating they can plastically increase a plants' tolerance of cold or arid conditions. However, maximum total NSCs increased, rather than decreased, with average site temperature and had no relationship to average site aridity. This result suggests that the total amount of NSC a plant stores may be more strongly determined by its capacity to assimilate carbon than by environmental stress. Thus, NSCs are unlikely to serve as reservoir of energy. This study is the most comprehensive synthesis to date of global NSC variation in relation to climate and supports the idea that NSC stores likely serve as buffers against environmental stress. By clarifying their role in cold and drought tolerance, we improve our ability to predict plant response to environment.
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Plant secondary metabolites that defend leaves from herbivores also occur in floral nectar. While specialist herbivores often have adaptations providing resistance to these compounds in leaves, many social insect pollinators are generalists, and therefore are not expected to be as resistant to such compounds. The milkweeds, Asclepias spp., contain toxic cardenolides in all tissues including floral nectar. We compared the concentrations and identities of cardenolides between tissues of the North American common milkweed Asclepias syriaca, and then studied the effect of the predominant cardenolide in nectar, glycosylated aspecioside, on an abundant pollinator. We show that a generalist bumblebee, Bombus impatiens, a common pollinator in eastern North America, consumes less nectar with experimental addition of ouabain (a standard cardenolide derived from Apocynacid plants native to east Africa) but not with addition of glycosylated aspecioside from milkweeds. At a concentration matching that of the maximum in the natural range, both cardenolides reduced activity levels of bees after four days of consumption, demonstrating toxicity despite variation in behavioral deterrence (i.e., consumption). In vitro enzymatic assays of Na+/K+-ATPase, the target site of cardenolides, showed lower toxicity of the milkweed cardenolide than ouabain for B. impatiens, indicating that the lower deterrence may be due to greater tolerance to glycosylated aspecioside. In contrast, there was no difference between the two cardenolides in toxicity to the Na+/K+-ATPase from a control insect, the fruit fly Drosophila melanogaster. Accordingly, this work reveals that even generalist pollinators such as B. impatiens may have adaptations to reduce the toxicity of specific plant secondary metabolites that occur in nectar, despite visiting flowers from a wide variety of plants over the colony’s lifespan.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/plphys/kiab131
