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DOE OSTI2023

Secreted Effector Proteins of Poplar Leaf Spot and Stem Canker Pathogen Sphaerulina musiva Manipulate Plant Immunity and Contribute to Virulence in Diverse Ways

We report fungal effectors play critical roles in manipulating plant immune responses and promoting colonization. Sphaerulina musiva is a heterothallic ascomycete fungus that causes Septoria leaf spot and stem canker disease in poplar (Populus spp.) plantations. This disease can result in premature defoliation, branch and stem breakage, increased mortality, and plantation failure. However, little is known about the interaction between S. musiva and poplar. Previous work predicted 142 candidate secreted effector proteins in S. musiva (SmCSEPs), 19 of which were selected for further functional characterization in this study. SmCSEP3 induced plant cell death in Nicotiana benthamiana, while 8 out of 19 tested SmCSEPs suppressed cell death. The signal peptides of these eight SmCSEPs exhibited secretory activity in a yeast signal sequence trap assay. Confocal microscopy revealed that four of these eight SmCSEPs target both the cytoplasm and the nucleus, whereas four predominantly localize to discrete punctate structures. Pathogen challenge assays in N. benthamiana demonstrated that the transient expression of six SmCSEPs promoted Fusarium proliferatum infection. The expression of these six SmCSEP genes were induced during infection. SmCSEP2, SmCSEP13, and SmCSEP25 suppressed chitin-triggered reactive oxygen species burst and callose deposition in N. benthamiana. The candidate secreted effector proteins of S. musiva target multiple compartments in the plant cell and modulate different pattern-triggered immunity pathways.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2024

Remarkably High Internal Transcribed Spacer Haplotype Diversity of the Fungal Select Agent Coniothyrium glycines Discovered Throughout Its Range in Sub-Saharan Africa

Red leaf blotch of soybean, caused by the fungus Coniothyrium glycines, is a foliar disease characterized by blotching, necrosis, and defoliation that has only been reported from Africa. The species is listed as a Select Agent by the Federal Select Agent Program due to its potentially devastating impacts to soybean production should it spread to the United States. Despite its potential import, very few isolates are available for study. Herein, we obtained 96 new C. glycines isolates from six soybean-producing countries throughout sub-Saharan Africa. Along with 12 previously collected ones, we sequenced each at the internal transcribed spacer (ITS) region. Between all isolates, we identified a total of 28 single-nucleotide polymorphisms and 23 haplotypes. One hypothesis to explain the tremendous diversity uncovered at the ITS—which is generally conserved within a species—is that our current species concept of C. glycines is too broad and that there may be multiple species that cause red leaf blotch. Zambia contained the highest haplotype diversity, a significant fraction of which remains unsampled. Most haplotypes were specific to a single country, except for two, which were found in Zambia and either neighboring Mozambique or Zimbabwe. This geographic specificity indicates that the ITS region may be useful for identifying source populations or routes of transmission should this pathogen spread beyond Africa. The observed geographic partitioning of this pathogen is likely the result of millions of years of replication on little-studied native hosts, given that soybean has only been cultivated in Africa since the early 1900s.

Plant Sciences↗

DOE OSTI2021

Canopy damage and recovery following Hurricane Maria using multitemporal lidar data, Mar/2017 - Mar/2020, Puerto Rico

Hurricane Maria (Category 4) snapped and uprooted canopy trees, removed large branches, and defoliated vegetation across Puerto Rico. The magnitude of forest damages and the rates and mechanisms of forest recovery following Maria provide important benchmarks for understanding the ecology of extreme events. We used airborne lidar data acquired before (2017) and after Maria (2018, 2020) to quantify landscape-scale changes in forest structure along a 439-ha elevational gradient (100 to 800 m) in the Luquillo Experimental Forest. Damages from Maria were widespread, with 73% of the study area losing ≥1 m in canopy height (mean = -7.1 m). Taller forests at lower elevations suffered more damage than shorter forests above 600 m. Yet only 13% of the study area had canopy heights ≤2 m in 2018, a typical threshold for forest gaps, highlighting the importance of damaged trees and advanced regeneration on post-storm forest structure. Heterogeneous patterns of regrowth and recruitment yielded shorter and more open forests by 2020. Nearly 45% of forests experienced initial height loss (<-1 m, 2017-2018) followed by rapid height gain (>1 m, 2018-2020), whereas 21.6% of forests with initial height losses showed little or no height gain, and 17.8% of forests exhibited no structural changes >|1| m in either period. Canopy layers <10 m accounted for most increases in canopy height and fractional cover between 2018-2020, with gains split evenly between height growth and lateral crown expansion by surviving individuals. These findings benchmark rates of gap formation, crown expansion, and canopy closure following hurricane damage. Included in the attached zip file are four TIF and four KML files.

54 ENVIRONMENTAL SCIENCES↗

DOE OSTI2021

AmeriFlux MX-PMm Puerto Morelos mangrove

This is the AmeriFlux version of the carbon flux data for the site MX-PMm Puerto Morelos mangrove. Site Description - The tower was located at the “Dr. Alfredo Barrera Marín” Botanical Garden. The surface monitored is covered with basin mangrove (sporadically flooded wetland) that grows in a fringe parallel to the northeastern coast (ca. 1 km) of the Yucatan Peninsula. The dominant species are Rhizophora mangle and Conocarpus erectus, which grow intertwined and relatively stunted (max tree height is 5m). Under the influence of trade winds and frequent stroms. The vegetation is regenerating after complete defoliation due to hurricane Wilma (cat. 4) passing in October 2005. The site is sporadically flooded by rainfall soil saturation excess; there are no marine surface water inputs but ground water level fluctuations show tidal signals. The terrain of the monitored surface is flat, while the area downwind of the tower presents a slope which corresponds to an ancient coast line. There is extensive urban development in the coastal dune along the coast mainly for tourism use (Mayan Riviera).

Alvarado-Barrientos, Ma. Susana↗

DOE OSTI2026

AmeriFlux FLUXNET-1F MX-PMm Puerto Morelos mangrove

This is the AmeriFlux Management Project (AMP) created FLUXNET-1F version of the carbon flux data for the site MX-PMm Puerto Morelos mangrove. This is the FLUXNET version of the carbon flux data for the site MX-PMm Puerto Morelos mangrove produced by applying the standard ONEFlux (1F) software. Site Description - The tower was located at the “Dr. Alfredo Barrera Marín” Botanical Garden. The surface monitored is covered with basin mangrove (sporadically flooded wetland) that grows in a fringe parallel to the northeastern coast (ca. 1 km) of the Yucatan Peninsula. The dominant species are Rhizophora mangle and Conocarpus erectus, which grow intertwined and relatively stunted (max tree height is 5m). Under the influence of trade winds and frequent stroms. The vegetation is regenerating after complete defoliation due to hurricane Wilma (cat. 4) passing in October 2005. The site is sporadically flooded by rainfall soil saturation excess; there are no marine surface water inputs but ground water level fluctuations show tidal signals. The terrain of the monitored surface is flat, while the area downwind of the tower presents a slope which corresponds to an ancient coast line. There is extensive urban development in the coastal dune along the coast mainly for tourism use (Mayan Riviera).

Alvarado-Barrientos, Ma. Susana [Instituto de Ecol↗

DOE OSTI2025

Remote Sensing Approach for Monitoring Tree Health Adjacent to Transmission Corridors

This study presents an initial proof-of-concept for a satellite-based remote sensing approach to identify and monitor potential areas of poor tree health across the entire BPA service territory on an annual basis. We tested three variants of “delta peak NDVI” ( ΔPN ) change detection metrics that express interannual variation in primary productivity relative to a baseline by comparing ΔPN values for known insect/disease disturbances and nearby reference locations. All three metrics showed promise for detecting poor tree health in the year during disturbance, but the metric based on the difference from the long-term (2016-2024) median ( Δ Med PN ) was preferred due to its responsiveness to change in the years during and after disturbance, resilience to interannual variation, and ease of interpretation as being above or below normal. Comparison of Δ Med PN grouped by relative severity of disturbance indicated it was not sensitive enough to detect “low” severity disturbances, as mapped by USGS’s LANDFIRE program, but could distinguish “moderate” and “high” severity disturbances from reference locations. These findings informed selection of a threshold for Δ Med PN , which was combined with areas exhibiting negative NDVI to map potential areas of concern. Visual inspection of before/after high-resolution imagery and NDVI time series showed that many areas of concern aligned with visible signs of defoliation and die-off as well as other types of disturbance (e.g., landslides, logging, road grading, flooding). Some areas of concern are thought to be false detections caused by persistent shadow, and some could not be explained with visual inspection due to spatiotemporal limitations of before/after imagery. In summary, our approach shows promise for large-scale monitoring of tree health adjacent to BPA transmission lines, but additional work is recommended to improve model sophistication and remove noise.

24 POWER TRANSMISSION AND DISTRIBUTION↗

DOE OSTI2023

Dynamic subcanopy leaf traits drive resistance of net primary production across a disturbance severity gradient

Across the globe, the forest carbon sink is increasingly vulnerable to an expanding array of low- to moderate-severity disturbances. However, some forest ecosystems exhibit functional resistance (i.e., the capacity of ecosystems to continue functioning as usual) following disturbances such as extreme weather events and insect or fungal pathogen outbreaks. Unlike severe disturbances (e.g., stand-replacing wildfires), moderate severity disturbances do not always result in near-term declines in forest production because of the potential for compensatory growth, including enhanced subcanopy production. Community-wide shifts in subcanopy plant functional traits, prompted by disturbance-driven environmental change, may play a key mechanistic role in resisting declines in net primary production (NPP) up to thresholds of canopy loss. However, the temporal dynamics of these shifts, as well as the upper limits of disturbance for which subcanopy production can compensate, remain poorly characterized. In this study, we leverage a 4-year dataset from an experimental forest disturbance in northern Michigan to assess subcanopy community trait shifts as well as their utility in predicting ecosystem NPP resistance across a wide range of implemented disturbance severities. Through mechanical girdling of stems, we achieved a gradient of severity from 0% (i.e., control) to 45, 65, and 85% targeted gross canopy defoliation, replicated across four landscape ecosystems broadly representative of the Upper Great Lakes ecoregion. We found that three of four examined subcanopy community weighted mean (CWM) traits including leaf photosynthetic rate (p = 0.04), stomatal conductance (p = 0.07), and the red edge normalized difference vegetation index (p < 0.0001) shifted rapidly following disturbance but before widespread changes in subcanopy light environment triggered by canopy tree mortality. Surprisingly, stimulated subcanopy production fully compensated for upper canopy losses across our gradient of experimental severities, achieving complete resistance (i.e., no significant interannual differences from control) of whole ecosystem NPP even in the 85% disturbance treatment. Additionally, we identified a probable mechanistic switch from nutrient-driven to light-driven trait shifts as disturbance progressed. Our findings suggest that remotely sensed traits such as the red edge normalized difference vegetation index (reNDVI) could be particularly sensitive and robust predictors of production response to disturbance, even across compositionally diverse forests. The potential of leaf spectral indices to predict post-disturbance functional resistance is promising given the capabilities of airborne to satellite remote sensing. We conclude that dynamic functional trait shifts following disturbance can be used to predict production response across a wide range of disturbance severities.

resistance↗

DOE OSTI2020

Stimulation of Insect Herbivory by Elevated Temperature Outweighs Protection by the Jasmonate Pathway

Rising global temperatures are associated with increases in the geographic range, population size, and feeding voracity of insect herbivores. Although it is well established that the plant hormone jasmonate (JA) promotes durable resistance to many ectothermic herbivores, little is known about how JA-mediated defense is influenced by rising temperatures. Here, we used the Arabidopsis-Trichoplusia ni (cabbage looper) interaction to investigate the relative contribution of JA and elevated temperature to host resistance. Video monitoring of T. ni larval behavior showed that elevated temperature greatly enhanced defoliation by increasing the bite rate and total time spent feeding, whereas loss of resistance in a JA-deficient mutant did not strongly affect these behaviors. The acceleration of insect feeding at elevated temperature was not attributed to decreases in wound-induced JA biosynthesis, expression of JA-responsive genes, or the accumulation of defensive glucosinolates prior to insect challenge. Quantitative proteomic analysis of insect frass, however, provided evidence for a temperature-dependent increase in the production of T. ni digestive enzymes. Our results demonstrate that temperature-driven stimulation of T. ni feeding outweighs the protective effects of JA-mediated resistance in Arabidopsis, thus highlighting a potential threat to plant resilience in a warming world.

59 BASIC BIOLOGICAL SCIENCES↗

DOE OSTI2023

Sensitivity of Optical Satellites to Estimate Windthrow Tree-Mortality in a Central Amazon Forest

Windthrow (i.e., trees broken and uprooted by wind) is a major natural disturbance in Amazon forests. Images from medium-resolution optical satellites combined with extensive field data have allowed researchers to assess patterns of windthrow tree-mortality and to monitor forest recovery over decades of succession in different regions. Although satellites with high spatial-resolution have become available in the last decade, they have not yet been employed for the quantification of windthrow tree-mortality. Here, we address how increasing the spatial resolution of satellites affects plot-to-landscape estimates of windthrow tree-mortality. We combined forest inventory data with Landsat 8 (30 m pixel), Sentinel 2 (10 m), and WorldView 2 (2 m) imagery over an old-growth forest in the Central Amazon that was disturbed by a single windthrow event in November 2015. Remote sensing estimates of windthrow tree-mortality were produced from Spectral Mixture Analysis and evaluated with forest inventory data (i.e., ground true) by using Generalized Linear Models. Field measured windthrow tree-mortality (3 transects and 30 subplots) crossing the entire disturbance gradient was 26.9 ± 11.1% (mean ± 95% CI). Although the three satellites produced reliable and statistically similar estimates (from 26.5% to 30.3%, p < 0.001), Landsat 8 had the most accurate results and efficiently captured field-observed variations in windthrow tree-mortality across the entire gradient of disturbance (Sentinel 2 and WorldView 2 produced the second and third best results, respectively). As expected, mean-associated uncertainties decreased systematically with increasing spatial resolution (i.e., from Landsat 8 to Sentinel 2 and WorldView 2). However, the overall quality of model fits showed the opposite pattern. We suggest that this reflects the influence of a relatively minor disturbance, such as defoliation and crown damage, and the fast growth of natural regeneration, which were not measured in the field nor can be captured by coarser resolution imagery. Our results validate the reliability of Landsat imagery for assessing plot-to-landscape patterns of windthrow tree-mortality in dense and heterogeneous tropical forests. Satellites with high spatial resolution can improve estimates of windthrow severity by allowing the quantification of crown damage and mortality of lower canopy and understory trees. However, this requires the validation of remote sensing metrics using field data at compatible scales.

54 ENVIRONMENTAL SCIENCES↗