Weak population differentiation and high diversity in Salsola tragus in the inland Pacific Northwest, USA.

BACKGROUND: Salsola tragus is a widespread and problematic weed of semi-arid wheat production globally, and in the inland Pacific Northwest region of the USA. The species exhibits high levels of phenotypic diversity across its range and, at least in California USA, previous work has described cryptic diversity comprising a multi-species complex. Such cryptic diversity could suggest the potential for a differential response to management inputs between groups, and have important implications for the spread of herbicide resistance or other adaptive traits within populations. We used a genotyping-by-sequencing approach to characterize the population structure of S. tragus in the inland Pacific Northwest. RESULTS: Our results indicated that the population in this region is comprised of a single, tetraploid species (S. tragus sensu latu) with weak population structure on a regional scale. Isolation-by-distance appears to be the primary pattern of structure, but an independent set of weakly differentiated clusters of unknown origin were also apparent, along with a mixed mating system and high levels of largely unstructured genetic diversity. CONCLUSIONS: Despite considerable phenotypic variability within S. tragus in the region, agronomic weed managers can likely consider it as a single entity across the region, rather than a collection of cryptic subgroups with possible differential responses to management inputs or agroecosystem conditions. A lack of strong barriers to migration and gene flow mean that adaptive traits, such as herbicide resistance, can be expected to spread rapidly through populations across the region. © 2022 Society of Chemical Industry.

On the hybrid origin of the C2 Salsola divaricata agg. (Amaranthaceae) from C3 and C4 parental lineages.

C2 photosynthesis is characterised using recapturing photorespiratory CO2 by RuBisCo in Kranz-like cells and is therefore physiologically intermediate between C3 and C4 photosynthesis. C2 can be interpreted as an evolutionary precursor of C4 and/or as the result of hybridisation between a C3 and C4 lineage. We compared the expression of photosynthetic traits among populations of the Salsola divaricata agg. (C2 ) from humid subtropical to arid habitats on the coasts of the Canary Islands and Morocco and subjected them to salt and drought treatments. We screened for enhanced C4 -like expression of traits related to habitat or treatment. We estimated species trees with a transcriptome dataset of Salsoleae and explored patterns of gene tree discordance. With phylogenetic networks and hybridisation analyses we tested for the hybrid origin of the Salsola divaricata agg. We observed distinct independent variation of photosynthetic traits within and among populations and no clear evidence for selection towards C4 -like trait expression in more stressful habitats or treatments. We found reticulation and gene tree incongruence in Salsoleae supporting a putative hybrid origin of the Salsola divaricata agg. C2 photosynthesis in the Salsola divaricata agg. combines traits inherited from its C3 and C4 parental lineages and seems evolutionarily stable, possibly well adapted to a wide climatic amplitude.

Germination heterochrony in annual plants of Salsola L.: an effective survival strategy in changing environments.

Germination heterochrony refers to germination of seeds dispersed in a single growing season, which is different from delayed germination. We studied two year's demographic characteristics, characteristics of fruit heteromorphism, the relationship between fruit heteromorphism and germination heterochrony, effects of moisture and temperature on germination characteristics, as well as seed longevity of four annual Salsola L. species to analyze the adaptive significance and causes of germination heterochrony. We found that the number of individuals of all populations changed drastically in one year. Approximately 41.6-100% of seedlings germinated in spring died. The number of fruit types varied with interspecies and intraspecies. Despite the wide range of germination temperature of different fruit types (0-35 °C), the germination percentage at 0-15 °C was the highest. When the soil moisture content was 20%, the germination percentage was the highest, reaching 50% within the shortest time. The contrary was the case with the decreasing of soil moisture. The seed longevity of the four species was one year. Fruit heteromorphism had no direct relationship to germination heterochrony. Germination heterochrony was caused by precipitation characteristics and short seed longevity of annual Salsola L., which was an effective survival strategy for plant to adapt to the changing environments in arid area.

Tripartite symbiosis of plant-weevil-bacteria is a widespread phenomenon in the Negev Desert.

The weevil Conorhynchus palumbus develops in a mud chamber affixed to the roots of the summer annual plant Salsola inermis in the Negev Desert of Israel. The weevil carries nitrogen fixing bacteria, and evidence suggests that plants with weevils utilize the fixed nitrogen. To characterize the distribution, abundance and significance of this unique interaction, we surveyed Salsola plants in 16 sites throughout the Negev Desert. We excavated ~100 plants from each site, recorded the presence of weevils in their roots, and characterized the soil properties in each site. Weevil mud chambers were present in all of the sampled sites and their abundance was positively correlated with soil nitrogen content and with plant size, and negatively correlated with soil grain-size. Intriguingly, we found two additional weevil species-Menecleonus virgatus and Maximus mimosae-residing in mud chambers on Salsola roots, and found one additional Salsola species-S. incanescens-accommodating weevils. Nitrogen fixing bacteria were found in weevil larvae of the two additional species and at multiple sites. Overall, our findings suggest that potentially beneficial associations between weevils and plants may be more common than previously acknowledged, and may play an important role in this desert ecosystem.

Identification of glyphosate resistance in Salsola tragus in north-eastern Oregon.

BACKGROUND: Farmers in the low-rainfall region of eastern Oregon rely on repeated applications of non-selective herbicides, predominately glyphosate, to control Salsola tragus in no-till fallow systems. Reports of poor glyphosate effectiveness have increased in recent years. Reduced efficacy is often attributed to dust, water stress, or generally poor growing conditions during application. Inadequate control also may be the result of the evolution of glyphosate resistance. Therefore, studies were undertaken to determine if glyphosate-resistant S. tragus populations occur in Oregon. RESULTS: Results from dose-response studies confirmed glyphosate resistance in three of 10 Oregon Salsola tragus populations. The ratio I50R /I50S from dose-response curves was, on average, 3.1 for the relative dry biomass per plant and 3.2 for the % of surviving plants per pot in these three populations. Plant mortality at recommended glyphosate doses for the resistant populations was less than 30% 3 weeks after treatment. CONCLUSIONS: Glyphosate resistance in S. tragus highlights the imperative need to diversify weed control strategies to preserve the longevity and sustainability of herbicides in semi-arid cropping systems of the Pacific Northwest. © 2017 Society of Chemical Industry.

Rapid range expansion of a newly formed allopolyploid weed in the genus Salsola.

PREMISE OF THE STUDY: Newly formed species (neospecies) can experience a variety of demographic fates, ranging from rapid invasive expansion to rapid extinction. Here we investigate the fate of the neospecies Salsola ryanii 10 years after its initial discovery in the Central Valley of California, USA. This species is an allopolyploid derived via hybridization between the invasive species, S. australis and S. tragus. METHODS: We conducted a systematic collection of Salsola species from 53 sites in California. Species-specific intersimple sequence repeat (ISSR) markers were used to determine the species of each individual collected. The range of S. ryanii identified in this study was compared to the range in 2002 to determine how the range has shifted in the decade between surveys. KEY RESULTS: In this survey, we identified 15 sites where S. ryanii was present (28% of sites), a significant population number increase since 2002. CONCLUSIONS: Salsola ryanii has undergone a dramatic population number expansion in the decade since it was originally documented. We are not aware of any plant neospecies whose range spontaneously experienced such a dramatic expansion. Salsola ryanii has every indication of being just as invasive as its highly invasive parents.

Salsola laricifolia, another C3-C 4 intermediate species in tribe Salsoleae s.l. (Chenopodiaceae).

This study identifies Salsola laricifolia as a C3-C4 intermediate in tribe Salsoleae s.l., Chenopodiaceae, and compares S. laricifolia with the previously described C3-C4 intermediates in Salsoleae. Photosynthetic pathway characteristics were studied in four species of this tribe including S. laricifolia, C3 Sympegma regelii, C3-C4 S. arbusculiformis, and C4 S. arbuscula, using the approaches of leaf anatomy and ultrastructure, activities of ribulose 1-5-bisphosphate carboxylase/oxygenase (Rubisco) and PEP carboxylase (PEPC), CO2 compensation point, and immunolocalization of Rubisco, PEPC, and the P-subunit of glycine decarboxylase (GDC). Salsola laricifolia has intermediate features, with near continuous and distinctive Kranz-like cells (KLCs) compared with the C3-Sympegmoid anatomical type and the C3-C4 intermediate S. arbusculiformis, a relatively low CO2 compensation point (30.4 µmol mol(-1)) and mesophyll (M)-to KLC tissue ratio, mitochondria in KLCs primarily occurring along the centripetal wall, and specific localization of P-protein GDC in the KLCs. The C3-type isotope value (-22.4 ‰), the absence of the clear labeling for PEPC in M cells, and the low activity of the PEPC enzyme (61.5 µmol mg(-1 )chlorophyll(-1) h(-1)) support the identification of S. laricifolia as a type I C3-C4 intermediate. Although these C3-C4 intermediate species have different structural features, one with discontinuous KL cells and the other with continuous, they have similar characteristics in physiology and biochemistry.

The acclimation of photosynthesis and respiration to temperature in the C3 -C4 intermediate Salsola divaricata: induction of high respiratory CO2 release under low temperature.

Photosynthesis in C(3) -C(4) intermediates reduces carbon loss by photorespiration through refixing photorespired CO(2) within bundle sheath cells. This is beneficial under warm temperatures where rates of photorespiration are high; however, it is unknown how photosynthesis in C(3) -C(4) plants acclimates to growth under cold conditions. Therefore, the cold tolerance of the C(3) -C(4) Salsola divaricata was tested to determine whether it reverts to C(3) photosynthesis when grown under low temperatures. Plants were grown under cold (15/10 °C), moderate (25/18 °C) or hot (35/25 °C) day/night temperatures and analysed to determine how photosynthesis, respiration and C(3) -C(4) features acclimate to these growth conditions. The CO(2) compensation point and net rates of CO(2) assimilation in cold-grown plants changed dramatically when measured in response to temperature. However, this was not due to the loss of C(3) -C(4) intermediacy, but rather to a large increase in mitochondrial respiration supported primarily by the non-phosphorylating alternative oxidative pathway (AOP) and, to a lesser degree, the cytochrome oxidative pathway (COP). The increase in respiration and AOP capacity in cold-grown plants likely protects against reactive oxygen species (ROS) in mitochondria and photodamage in chloroplasts by consuming excess reductant via the alternative mitochondrial respiratory electron transport chain.

Tri-party underground symbiosis between a weevil, bacteria and a desert plant.

Inhabitants of arid ecosystems face severe nitrogen and water limitations. Inventive adaptations by organisms occupying such habitats are essential for survival. This study describes a tri-party symbiotic interaction between a plant (Salsola inermis), a beetle (Conorhynchus pistor), and a bacterium (Klebsiella pneumonia). The weevil survives by living within a mud structure affixed to the plant roots, thus benefiting from increased carbon and water, and refuge from predators and parasites. Active nitrogen-fixing bacteria harbored within the weevil's gut mediate this interaction, by supplying nitrogen to the system, which eventually promotes seed development. We studied the correlation between the weevil's existence and (i) root carbon and nitrogen content, (ii) soil water content and (iii) seed weight. Roots hosting weevils contained more nitrogen, heavier seeds and less carbon. In addition, water content was higher around the roots than in open spaces a short distance from the plant stem. Bacterial studies and nitrogen-fixation analyses, including molecular and chemical assays, indicated atmospheric nitrogen fixation in the larval stage and identified the bacterium. The coexistence of weevil and bacterial behavior coinciding with the plant's life cycle was revealed here by a long period of field observations. Out of over 60,000 known weevils, this is the only report of a weevil living most of its life underground without harming plants. The unique tri-party interaction described herein shows the important ecological role of desert plant roots and provides an example of a sustainable consortium of living organisms coping with the challenging desert environment.

Does an expressed sequence tag (EST) library of Salsola iberica (tumbleweed) help to understand plant responses to environmental stresses?

Weeds play an important role in agriculture and molecular techniques are useful to help understand traits that contribute to weediness and weeds' interactions with the environment. A total of 377 expressed sequence tags (ESTs) from a modest library were arranged into 227 unique fragments and 61 contigs, which consisted of two or more ESTs. From blastx results, we mapped and annotated unigenes using the gene ontology vocabulary according to biological process, cellular component and molecular function. These were then compared to a reference set of Arabidopsis thaliana sequences for statistically significant over- or underrepresented genes. The sequences were also compared against multiple protein databases for similarity of functional domains. Overall, the S. iberica sequences showed high similarity to response to stress, which included salt-induced proteins, betaine aldehydehyde dehydrogenase and calcium binding proteins. Only a modest number of transcripts were sequenced; however, the results presented here demonstrate the metabolic versatility of S. iberica in sub-optimal conditions that are likely to contribute to its cosmopolitan distribution. Here we propose that an EST library of an economically important weed species could be used to understand the weed's interactions with the environment.

Salt-driven interactions between Pistacia lentiscus and Salsola inermis.

BACKGROUND, AIM, AND SCOPE: It can be learned from the Pistacia spp. germplasm collection (http://www.bgu.ac.il/pistacia) that the growth of Salsola inermis is inhibited in the vicinity of the evergreen Pistacia lentiscus, but not in the surroundings of the deciduous Pistacia atlantica and Pistacia chinensis. Irrigation of trees during the summer months increases soil salinity around the trees. It was therefore hypothesized that inhibition of S. inermis around P. lentiscus is related to depletion of salt in the vicinity of the latter species. MATERIALS AND METHODS: A multi-approach experimental scheme was carried out which included soil edaphic characterization and germination tests. To test salt tolerance of P. lentiscus, plants were grown in a hydroponic system for a month in medium containing NaCl, while physiological and growth parameters were measured. RESULTS: Conductivity measurements in summer, during the growth season of S. inermis, indicated that soil salinity beneath deciduous Pistacia trees was significantly higher than that below P. lentiscus. Germination of S. inermis seeds on filter paper moistened with P. lentiscus low-conductivity soil filtrate was twice as high as that of the deciduous trees high-conductivity soil filtrates. Nevertheless, fresh and dry weights of mature S. inermis growing next to P. atlantica and P. chinensis were 2.9 to 4.8 times higher than those of plants growing in the vicinity of P. lentiscus. In a hydroponic system, no significant differences were found in growth parameters and stomatal conductance between P. lentiscus growing in control and salt treatments. It was therefore proposed that salt depletion in the vicinity of P. lentiscus inhibits the growth, but not germination, of S. inermis thus confirming the halophylic characteristics of this plant. DISCUSSION: The nature of Salsola-Pistacia interactions cannot be explained by allelopathic effects; hence, plausible salt-driven interactions were considered. Our data showed that S. inermis accumulated salt and has halophytic characteristics. Interestingly, germination of S. inermis was inhibited in medium containing salt, but the salt was obligatory for further growth, development, and fast biomass production. These results explained the observation of large biomass accumulation in the more saline soil around the deciduous P. atlantica and P. chinensis and the lack of development in the salt-depleted soil around the salt-tolerant accumulator P. lentiscus. CONCLUSIONS: Soil salinity around Pistacia trees critically affects the growth of S. inermis. Inhibition of S. inermis growth, but not germination, around the evergreen P. lentiscus, stems from the latter's ability to deplete salt from its surroundings. The results indicated that P. lentiscus is able to tolerate and accumulate salt, which we assume contributes to its wide distribution along the Mediterranean coast in Israel. Recommendations and perspectives While the phytoremediation potential of Salsola spp. has been explored to some extent, this of P. lentiscus has not been tested and proven before. The results suggest that the evergreen perennial salt-tolerant P. lentiscus can be recommended for horticulture purposes and soil stabilization in relatively saline environments.