Seed fungal endophytes promote the establishment of invasive <i>Poa annua</i> in maritime Antarctica

Ballesteros, Gabriel I.; Acuña‐Rodríguez, Ian S.; Barrera, Andrea; Gundel, Pedro E.; Newsham, Kevin K.; Molina‐Montenegro, Marco A.

doi:10.1080/17550874.2022.2145579

Cited by 6 publications

(12 citation statements)

References 81 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…One group was maintained as seeds with fungal endophytes, while the other group, hereafter referred to as E − , was submersed in the fungicide Benlate® (2 g L −1 ; DuPont) for 30 min at room temperature to remove endophytes. Benlate has a broad spectrum of action and is harmless to the seeds of Antarctic plants (Ballesteros et al, 2022; Barrera et al, 2020; Hereme et al, 2020). Hence, three different groups of seeds (E + , E 0 and E − ) were obtained at the start of the experiment.…”

Section: Methodsmentioning

confidence: 99%

“…Clothing or cargo is considered to be the main vectors for the introduction of seeds and other propagules from other continents (Chown et al, 2012; Hughes et al, 2010; Huiskes et al, 2014). Although P. annua has been eradicated from most of the locations in which it has been discovered, on King George Island (South Shetland Islands, 62° S), where the founder population was initially left uncontrolled, the species has rapidly invaded local natural tundra, where it competes vigorously with the two native Antarctic vascular plant species, Deschampsia antarctica and Colobanthus quitensis (Molina‐Montenegro et al, 2019; Olech & Chwedrozewska, 2011), negatively impacting their biomass, fecundity and survival (Ballesteros et al, 2022; Cavieres et al, 2018; Molina‐Montenegro et al, 2012, 2019). However, despite the successful establishment of P. annua in Maritime Antarctica, and the threat posed by the species to the conservation of native vascular plants, the mechanisms underlying its environmental tolerance and competitiveness in the region have seldom been assessed (but see Ballesteros et al, 2022; Pertierra et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

“…Several studies indicate that beneficial symbioses with fungal endophytes that colonize seeds and are transmitted vertically between generations may allow vascular plants to survive harsh Antarctic environmental conditions (Acuña‐Rodríguez et al, 2020; Barrera et al, 2020; Hereme et al, 2020). A recent study has shown that the release of allelochemicals – chiefly phenolic compounds – by seed endophytes of P. annua negatively affect the biomass and fecundity of D. antarctica and C. quitensis , possibly enhancing the competitiveness of P. annua in the natural environment (Ballesteros et al, 2022). Although the role of biotic interactions in mediating plant invasions is now well established, the role of endophytes in this regard remains poorly studied (but see Traveset & Richardson, 2020).…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

The “Trojan horse” strategy: Seed fungal endophyte symbiosis helps to explain the invasion success of the grass, Poa annua, in Maritime Antarctica

Molina‐Montenegro,

Ballesteros,

Acuña‐Rodríguez

et al. 2023

Diversity and Distributions

Self Cite

View full text Add to dashboard Cite

AimPoa annua L. (annual bluegrass) is presently the sole invasive vascular plant species to have successfully established in Maritime Antarctica, where it poses a significant conservation threat to native plant species. However, the reasons for its success in the region have yet to be established. Here, we determined whether the invasiveness of P. annua, and its competitiveness with the native Antarctic hairgrass Deschampsia antarctica, is influenced by symbioses formed with seed fungal endophytes, and whether plants derived from seeds from four global regions differ in their performance.LocationsFour regions (Maritime Antarctica, sub‐Antarctica, South America and Europe).MethodsEndophyte frequency was measured in P. annua seeds collected from the four regions. The germination, survival, biomass accumulation, flowering and competitiveness with D. antarctica of P. annua plants grown from endophyte‐uncolonised and uncolonised seeds was determined in the laboratory. The effects of endophytes on P. annua seed germination and survival and seedling osmoprotection were also assessed in the Maritime Antarctic natural environment using locally‐sourced seeds.ResultsEndophytes were at least twice as frequent in seeds from Maritime Antarctica than in those from other regions. A higher proportion of endophyte‐colonized seeds germinated and survived than did uncolonised seeds, but only when they originated from Maritime Antarctica. Seed endophytes increased the competitiveness of P. annua with D. antarctica, but only for plants grown from Maritime Antarctic seeds. In the field, endophyte‐colonized seeds from Maritime Antarctica germinated and survived more frequently than uncolonised seeds, and osmoprotection was higher in seedlings grown from colonized seed.Main ConclusionsThe findings indicate beneficial effects of seed endophytes on invasion‐related traits of P. annua, such as survival, germination success and flowering. Together with vegetative and reproductive traits facilitating the colonization process, the seed‐fungal endophyte symbiosis can be invoked as an important factor explaining the invasiveness of P. annua in Maritime Antarctica.

show abstract

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

The “Trojan horse” strategy: Seed fungal endophyte symbiosis helps to explain the invasion success of the grass, Poa annua, in Maritime Antarctica

Molina‐Montenegro,

Ballesteros,

Acuña‐Rodríguez

et al. 2023

Diversity and Distributions

Self Cite

View full text Add to dashboard Cite

show abstract

“…Leaf phenol and proline concentrations and lipid peroxidation were measured in three fully expanded leaves from 25 randomly selected plants in each experimental group at the end of each experiment in 2021. Total leaf phenolic compound concentrations were determined spectrophotometrically using the Folin-Ciocalteu method and expressed as μmol phenols g À1 fresh weight, as described by Ballesteros et al (2022). Phenolic compounds in plant tissues provide antioxidant capacity by scavenging free radicals and reactive oxygen species (ROS) associated with abiotic stresses and are thus an important indicator of plant health (Shi et al, 2022).…”

Section: Biochemical Mechanisms Of Environmental Tolerancementioning

confidence: 99%

Extreme environments as sources of fungal endophytes mitigating climate change impacts on crops in Mediterranean‐type ecosystems

Ballesteros,

Newsham,

Acuña‐Rodríguez

et al. 2023

Plants People Planet

Self Cite

View full text Add to dashboard Cite

Societal Impact StatementClimate change is predicted to increase drought and soil salinity in Mediterranean‐type ecosystems (MTEs), posing a significant threat to global food security. Genetic modification of crops to counteract this threat is expensive and has not met with universal support, and alternatives are hence needed to enhance crop production in MTEs. Here, fungal endophytes from the Atacama Desert, High Andes and Antarctica inoculated onto three crops were found to alleviate the negative effects of drought and salinity on plant performance. The study concludes that extremophile endophytes might be used to enhance crop performance as the climate of MTEs changes over future decades.Summary Climate change will curtail the ability to provide sufficient food for our rapidly expanding population. Improvements to crop production in changing environments, particularly Mediterranean‐type ecosystems (MTEs), which are increasingly subjected to drought and salinisation, are hence urgently needed. Here, we explored the possibility that fungal endophytes from extreme environments can be used to enhance crop yield, survival and tolerance to environmental stresses. Plants of lettuce, tomato and bell pepper were inoculated with up to six species of endophytic fungi isolated from the Atacama Desert, the High Andes and Antarctica. They were then exposed in the field for up to 120 days in each of three summers to current climatic conditions or to a future climate scenario simulating increased drought and soil salinisation. Compared with uninoculated plants, the yield and survival of inoculated crops were increased by up to two‐fold under the future climate scenario. These effects were in part attributable to the improved water balance of inoculated crops exposed to drought and salinisation. The inocula also increased the concentrations of total phenols and proline in leaves and decreased lipid peroxidation when plants were subjected to increased aridity and salinity. A mixed inoculum of six endophytes from the extreme environments conferred the most beneficial effects on crop performance, with a commercially available inoculum having fewer positive effects on crops. We conclude that the inoculation of crops with endophytes from extreme environments may be a viable solution to sustaining crop production in MTEs exposed to rapid climate change.

show abstract

“…Unlike mycorrhizal fungi, very little is known about how foliar endophyte fungi influence the success of invasive forbs [ 23 ], though clavicipitaceous endophytes are often implicated in the invasion success of grasses [ 24 ]. Indeed, one recent example suggests that endophytes have facilitated the invasion success of the annual grass Poa annua in Antarctica [ 25 ]. This knowledge gap is despite the fact that Evans [ 26 ] proposed the endophyte–enemy release hypothesis, in which it was postulated that invasive plants may be introduced with their co-evolved endophytes, giving them protection against any local natural enemies, leading to enhanced competitive success [ 27 ].…”

Section: Introductionmentioning

confidence: 99%

The Invasive Plant Impatiens glandulifera Manipulates Microbial Associates of Competing Native Species

Razak

Gange

Sutton

et al. 2023

Plants

View full text Add to dashboard Cite

Impatiens glandulifera or Himalayan balsam is one of the most invasive weeds across Europe and can seriously reduce native plant diversity. It often forms continuous monocultures along river banks, but the mechanisms of this arrested succession are largely unknown. Here, we investigated the effect of arbuscular mycorrhizal (AM) fungi on balsam competitive ability with two native plant species, Plantago lanceolata and Holcus lanatus. We also studied how competition with Impatiens affects colonisation by foliar endophytes and mycorrhizas of two other co-occurring native species, Urtica dioica and Cirsium arvense. Mycorrhizal colonisation reduced balsam growth when the plants were grown singly, but appeared to have little effect when balsam experienced intra- or interspecific competition. Competition with balsam together with the addition of mycorrhizas had no effect on P. lanceolata biomass, suggesting that the fungi were beneficial to the latter, enabling it to compete effectively with balsam. However, this was not so with H. lanatus. Meanwhile, competition with Impatiens reduced endophyte numbers and mycorrhizal colonisation in U. dioica and C. arvense, leading to enhanced susceptibility of these plants to insect attack. Himalayan balsam is known to degrade soil fungal populations and can also reduce foliar beneficial fungi in neighbouring plants. This allows the plant to compete effectively with itself and other native species, thereby leading to the continuous monocultures.

show abstract

Seed fungal endophytes promote the establishment of invasive Poa annua in maritime Antarctica

Cited by 6 publications

References 81 publications

The “Trojan horse” strategy: Seed fungal endophyte symbiosis helps to explain the invasion success of the grass, Poa annua, in Maritime Antarctica

The “Trojan horse” strategy: Seed fungal endophyte symbiosis helps to explain the invasion success of the grass, Poa annua, in Maritime Antarctica

Extreme environments as sources of fungal endophytes mitigating climate change impacts on crops in Mediterranean‐type ecosystems

The Invasive Plant Impatiens glandulifera Manipulates Microbial Associates of Competing Native Species

Contact Info

Product

Resources

About