Mycorrhizas in South American Ericaceae.

Mycorrhizal symbioses (mycorrhizas) of Ericaceae, including ericoid mycorrhiza (ErM), have been mainly studied in the Northern Hemisphere, although the highest diversity of ericaceous plants is located in the Southern Hemisphere, where several regions remain largely unexplored. One of them is South America, which harbors a remarkably high diversity of Ericaceae (691 species and 33 genera) in a wide range of environmental conditions, and a specific mycorrhizal type called cavendishioid. In this review, we compile all available information on mycorrhizas of Ericaceae in South America. We report data on the mycorrhizal type and fungal diversity in 17 and 11 ericaceous genera, respectively. We show that South American Ericaceae exhibit a high diversity of habitats and life forms and that some species from typical ErM subfamilies may also host arbuscular mycorrhiza. Also, a possible geographical pattern in South American ErM fungal communities is suggested, with Sebacinales being the dominant mycorrhizal partners of the Andean clade species from tropical mountains, while archetypal ErM fungi are common partners in southern South America species. The gathered information challenges some common assumptions about ErM and suggests that focusing on understudied regions would improve our understanding of the evolution of mycorrhizal associations in this intriguing family.

Cluster roots of Embothrium coccineum modify their metabolism and show differential gene expression in response to phosphorus supply.

Embothrium coccineum produces cluster roots (CR) to acquire sparingly soluble phosphorus (P) from the soil through the exudation of organic compounds. However, the physiological mechanisms involved in carbon drainage through its roots, as well as the gene expression involved in the biosynthesis of carboxylates and P uptake, have not been explored. In this work, we evaluated the relationship between carboxylate exudation rate and phosphoenolpyruvate carboxylase (PEPC) activity in roots of E. coccineum seedlings grown in a nutrient-poor volcanic substrate. Second, we evaluated CR formation and the expression of genes involved in the production of carboxylates (PEPC) and P uptake (PHT1) in E. coccineum seedlings grown under three different P supplies in hydroponic conditions. Our results showed that the carboxylate exudation rate was higher in CR than in non-CR, which was consistent with the higher PEPC activity in CR. We found higher CR formation in seedlings grown at 5 µM of P supply, concomitant with a higher expression of EcPEPC and EcPHT1 in CR than in non-CR. Overall, mature CR of E. coccineum seedlings growing on volcanic substrates poor in nutrients modify their metabolism compared to non-CR, enhancing carboxylate biosynthesis and subsequent carboxylate exudation. Additionally, transcriptional responses of EcPEPC and EcPHT1 were induced simultaneously when E. coccineum seedlings were grown in P-limited conditions that favored CR formation. Our results showed, for the first time, changes at the molecular level in CR of a species of the Proteaceae family, demonstrating that these root structures are highly specialized in P mobilization and uptake.

Photosynthetic metabolism during phosphate limitation in a legume from the Mediterranean-type Fynbos ecosystem.

Phosphorus (P) is an essential mineral, required for crucial plant genetic, metabolic and signaling functions. Under P deficiency, normal physiological function can be disrupted, especially photosynthetic metabolism. The majority of photosynthetic studies of P stress has been on model organisms, and very little is known about plants that evolved on P deficient soils. Aspalathus linearis (Burm.f.) R.Dahlgren, a native to the Mediterranean ecosystem of South Africa was used to study the photosynthetic responses during short-term P limitation. A. linearis seedlings were cultured under glasshouse conditions and exposed to short-term P stress. Leaf photosynthetic gas exchange was coupled with metabolic analyses. In spite of the decline in leaf cellular Pi, the photosynthetic rates remained unchanged. These leaves also maintained their levels of light harvesting and reaction center pigments. The efficiency of the light reactions' utilization of ATP and NADPH increased during P-stress. Leaf glucose levels decreased during P-stress, while sucrose concentrations remained unaffected. These results show that during short-term P-stress, A. linearis can maintain its photosynthetic rates by altering the structural and functional components of the light reactions.

Nutrient Use Efficiency of Southern South America Proteaceae Species. Are there General Patterns in the Proteaceae Family?

Plants from the Proteaceae family can thrive in old, impoverished soil with extremely low phosphorus (P) content, such as those typically found in South Western Australia (SWA) and South Africa. The South Western (SW) Australian Proteaceae species have developed strategies to deal with P scarcity, such as the high capacity to re-mobilize P from senescent to young leaves and the efficient use of P for carbon fixation. In Southern South America, six Proteaceae species grow in younger soils than those of SWA, with a wide variety of climatic and edaphic conditions. However, strategies in the nutrient use efficiency of Southern South (SS) American Proteaceae species growing in their natural ecosystems remain widely unknown. The aim of this study was to evaluate nutrient resorption efficiency and the photosynthetic nutrients use efficiency by SS American Proteaceae species, naturally growing in different sites along a very extensive latitudinal gradient. Mature and senescent leaves of the six SS American Proteaceae species (Embothrium coccineum, Gevuina avellana, Orites myrtoidea Lomatia hirsuta, L. ferruginea, and L. dentata), as well as, soil samples were collected in nine sites from southern Chile and were subjected to chemical analyses. Nutrient resorption (P and nitrogen) efficiency in leaves was estimated in all species inhabiting the nine sites evaluated, whereas, the photosynthetic P use efficiency (PPUE) and photosynthetic nitrogen (N) use efficiency (PNUE) per leaf unit were determined in two sites with contrasting nutrient availability. Our study exhibit for the first time a data set related to nutrient use efficiency in the leaves of the six SS American Proteaceae, revealing that for all species and sites, P and N resorption efficiencies were on average 47.7 and 50.6%, respectively. No correlation was found between leaf nutrient (P and N) resorption efficiency and soil attributes. Further, different responses in PPUE and PNUE were found among species and, contrary to our expectations, a higher nutrient use efficiency in the nutrient poorest soil was not found. We conclude that SS American Proteaceae species did not show a general pattern in the nutrient use efficiency among them neither with others Proteaceae species reported in the literature.

Carbon allocation to growth and storage in two evergreen species of contrasting successional status.

PREMISE OF THE STUDY: A prevailing hypothesis in forest succession is that shade-tolerant species grow more slowly than shade-intolerant species, across light conditions, because they prioritize carbon (C) allocation to storage. We examined this hypothesis in a confamilial pair of species, including one of the fastest-growing tree species in the world (Eucalyptus globulus) and a shade-tolerant, slow-growing species (Luma apiculata). METHODS: Seedlings were subjected to one out of four combinations of light (high vs. low) and initial defoliation (90% defoliated vs. nondefoliated) for four months. Growth, C storage concentration in different organs, leaf shedding, and lateral shoot formation were measured at the end of the experiment. KEY RESULTS: Eucalyptus globulus grew faster than L. apiculata in high light, but not in low light. Both species had lower C storage concentration in low than in high light, but similar C storage concentrations in each light condition. Defoliation had no effect on C storage, except in the case of the old leaves of both species, which showed lower C storage levels in response to defoliation. Across treatments, leaf shedding was 96% higher in E. globulus than in L. apiculata while, in contrast, lateral shoot formation was 87% higher in L. apiculata. CONCLUSIONS: In low light, E. globulus prioritized C storage instead of growth, whereas L. apiculata prioritized growth and lateral branching. Our results suggest that shade tolerance depends on efficient light capture rather than C conservation traits.

Physiological and morphological responses to permanent and intermittent waterlogging in seedlings of four evergreen trees of temperate swamp forests.

Waterlogging decreases a plant's metabolism, stomatal conductance (gs) and photosynthetic rate (A); however, some evergreen species show acclimation to waterlogging. By studying both the physiological and morphological responses to waterlogging, the objective of this study was to assess the acclimation capacity of four swamp forest species that reside in different microhabitats. We proposed that species (Luma apiculata [D.C.] Burret. and Drimys winteri J.R. et G. Forster.) abundant in seasonally and intermittently waterlogged areas (SIWA) would have a higher acclimation capacity than species abundant in the inner swamp (Blepharocalyx cruckshanksii [H et A.] Mied. and Myrceugenia exsucca [D.C.] Berg.) where permanent waterlogging occurs (PWA); it was expected that the species from SIWA would maintain leaf expansion and gas exchange rates during intermittent waterlogging treatments. Conversely, we expected that PWA species would have higher constitutive waterlogging tolerance, and this would be reflected in the formation of lenticels and adventitious roots. Over the course of 2 months, we subjected seedlings to different waterlogging treatments: (i) permanent (sudden, SW), (ii) intermittent (gradual) or (iii) control (field capacity, C). Survival after waterlogging was high (≥80%) for all species and treatments, and only the growth rate of D. winteri subjected to SW was affected. Drimys winteri plants had low, but constant A and g during both waterlogging treatments. Conversely, L. apiculata had the highest A and g values, and g increased significantly during the first several days of waterlogging. In general, seedlings of all species subjected to waterlogging produced more adventitious roots and fully expanded leaves and had higher specific leaf area (SLA) and stomatal density (StD) than seedlings in the C treatment. From the results gathered here, we partially accept our hypothesis as all species showed high tolerance to waterlogging, maintained growth, and had increased A or g during different time points of waterlogging. Differences in leaf (SLA) and stomata functioning (gs, StD) plasticity likely allows plants to maintain positive carbon gains when waterlogging occurs. The species-specific differences found here were not entirely related to microhabitat distribution.

Soil nitrogen, and not phosphorus, promotes cluster-root formation in a South American Proteaceae, Embothrium coccineum.

PREMISE OF THE STUDY: Cluster roots are a characteristic root adaptation of Proteaceae species. In South African and Australian species, cluster roots promote phosphorus (P) acquisition from poor soils. In a South American Proteaceae species, where cluster roots have been scarcely studied and their function is unknown, we tested whether cluster-root formation is stimulated by low soil nutrition, in particular low P-availability. METHODS: Small and large seedlings (< 6- and > 6-months old, respectively) of Embothrium coccineum and soil were collected across four different sites in Patagonia (Chile). We determined cluster-root number and relative mass, and leaf Pi concentration per mass (Pimass) and per area (Piarea) for each seedling, and tested relationships with Olsen-P (OP), sorbed-P (sP) and total nitrogen (N) using generalized linear mixed-effects models and model selection to assess the relative strength of soil and plant drivers. KEY RESULTS: Best-fit models showed a negative logarithmic relationship between cluster-root number and soil nitrogen (N), and between cluster-root relative mass and both leaf Piarea and soil N, and a positive logarithmic relationship between cluster-root number and leaf Piarea. Cluster-root relative mass was higher in small than in large seedlings. CONCLUSIONS: Contrary to that found in South African and Australian Proteaceae, cluster roots of E. coccineum do not appear to be driven by soil P, but rather by soil N and leaf Piarea. We suggest that cluster roots are a constitutive and functional trait that allows plants to prevail in poor N soils.

Phosphorus-mobilization ecosystem engineering: the roles of cluster roots and carboxylate exudation in young P-limited ecosystems.

BACKGROUND: Carboxylate-releasing cluster roots of Proteaceae play a key role in acquiring phosphorus (P) from ancient nutrient-impoverished soils in Australia. However, cluster roots are also found in Proteaceae on young, P-rich soils in Chile where they allow P acquisition from soils that strongly sorb P. SCOPE: Unlike Proteaceae in Australia that tend to proficiently remobilize P from senescent leaves, Chilean Proteaceae produce leaf litter rich in P. Consequently, they may act as ecosystem engineers, providing P for plants without specialized roots to access sorbed P. We propose a similar ecosystem-engineering role for species that release large amounts of carboxylates in other relatively young, strongly P-sorbing substrates, e.g. young acidic volcanic deposits and calcareous dunes. Many of these species also fix atmospheric nitrogen and release nutrient-rich litter, but their role as ecosystem engineers is commonly ascribed only to their diazotrophic nature. CONCLUSIONS: We propose that the P-mobilizing capacity of Proteaceae on young soils, which contain an abundance of P, but where P is poorly available, in combination with inefficient nutrient remobilization from senescing leaves allows these species to function as ecosystem engineers. We suggest that diazotrophic species that colonize young soils with strong P-sorption potential should be considered for their positive effect on P availability, as well as their widely accepted role in nitrogen fixation. Their P-mobilizing activity possibly also enhances their nitrogen-fixing capacity. These diazotrophic species may therefore facilitate the establishment and growth of species with less-efficient P-uptake strategies on more-developed soils with low P availability through similar mechanisms. We argue that the significance of cluster roots and high carboxylate exudation in the development of young ecosystems is probably far more important than has been envisaged thus far.

Environmental factors affect the spatial arrangement of survival and damage of outplanted nothofagus dombeyi seedlings in the chilean andes / Factores ambientales afectan el arreglo espacial de la sobrevida y daño en plantas transplantadas de nothofagus dombeyi en los andes chilenos / Fatores ambientais afetam o arranjo espacial da sobrevida e dano em plantas transplantadas de nothofagus dombeyi nos andes chilenos

Mortality patterns were analyzed in a one-year old Nothofagus dombeyi plantation at mid-elevation in the Chilean Andes. Ripley´s univariate function was used to detect spatial patterns of mortality and damage (as reflected in crown dieback) of seedlings by assigning them into four categories: no crown damage, 1/3 of the crown damaged, 2/3 of the crown damaged and dead. Through correspondence analysis, variables (plant attributes, topography, weed competition, neighboring vegetation and fertilization) that could affect mortality were tested. At the end of the first growing season 67% of the seedlings survived, and by the end of the following dormant season only 37% were alive. Mortality patterns were random for seedlings with 1/3 of the crown damaged, and clustered for all other categories. Environmental variables with the greatest influence on mortality were increasing distance to a neighboring 10m tall plantation, absence of tall vegetation cover and convex micro-topography. Results suggest that large temperature oscillations with events of freezing temperatures (defined as the reported lethal temperature for 50% of its leaves) during the growing season, and severe frost during the dormant season, were the main causes of mortality and damage. The convenience of providing seedlings with some shelter when outplanted, or with an appropriate cold-acclimation treatment to resist low freezing temperatures when outplanted in open fields in harsh cold regions of the south-central Andes is discussed.

Se analizaron los patrones de mortandad en una plantación de Nothofagus dombeyi de un año de edad a altura media en los Andes chilenos. La función univariada de Ripley fue utilizada para detectar patrones espaciales de mortalidad y daño de las plantas asumiendo cuatro categorías: sin daño en la copa, 1/3 de copa dañada, 2/3 de copa dañada y muerte. Las variables (atributos de la planta, topografía, competencia de maleza, vegetación vecina y fertilización) fueron probadas por análisis de correspondencia. Al final de la primera estación de crecimiento 67% de las plantas sobrevivieron y al final del siguiente período latente solo 37% sobrevivían. Los patrones de mortalidad fueron aleatorios en plantas con 1/3 de la copa dañada, y agrupados en las otras tres categorías. Las variables ambientales con la mayor influencia en mortalidad fueron: distancia a una plantación vecina de 10m de altura, ausencia de cobertura vegetal alta y microtopografía convexa. Los resultados sugieren que grandes variaciones de temperatura con eventos de congelamiento (definido como la temperatura reportada como letal para 50% de las hojas) en la estación de crecimiento y congelamiento severo en la estación de latencia fueron las causas principales de mortalidad y daño. Se discute la conveniencia de proteger las plantaciones transplantadas o de una aclimatación apropiada para resistir las bajas temperaturas en plantas transplantadas a campo abierto en zonas frías de los Andes chilenos sur-centrales.

Analisaram-se os padrões de mortalidade em uma plantação de Nothofagus dombeyi de um ano de idade a altura média nos Andes chilenos. A função univariada de Ripley foi utilizada para detectar padrões espaciais de mortalidade e dano das plantas assumindo quatro categorias: sem dano na coroa, 1/3 de coroa danificada, 2/3 de coroa danificada e morte. As variáveis (atributos da planta, topografia, competência de maleza, vegetação vizinha e fertilização) foram provadas por análise de correspondência. No final da primeira estação de crescimento 67% das plantas sobreviveram e no final do seguinte período latente somente 37% sobreviviam. Os padrões de mortalidade foram aleatórios em plantas com 1/3 da coroa danificada, e agrupados nas outras três categorias. As variáveis ambientais com a maior influência em mortalidade foram: distância a uma plantação vizinha de 10m de altura, ausência de cobertura vegetal alta e microtopografía convexa. Os resultados sugerem que grandes variações de temperatura com momentos de congelamento (definido como a temperatura relatada como letal para 50% das folhas) na estação de crescimento e, congelamento severo na estação de latência, foram as causas principais de mortalidade e dano. Discute-se a conveniência de proteger as plantações transplantadas ou de uma aclimatação apropriada para resistir as baixas temperaturas em plantas transplantadas a campo aberto em zonas frias dos Andes chilenos sul-centrais.

Arabidopsis thaliana avoids freezing by supercooling.

Arabidopsis thaliana (L.) Heynh. has been described as a freezing-tolerant species based on freezing-resistance assays. Nonetheless, this type of experiment does not discriminate between freezing-tolerance and freezing-avoidance mechanisms. The purpose of this paper was to determine which of these two freezing-resistance mechanisms is responsible for freezing resistance in A. thaliana. This was achieved by comparing the thermal properties (ice-nucleation temperature and the freezing temperature) of leaves and the lethal temperature to 10, 50 and 90% of the plants (LT10, LT50, and LT90, respectively). Two wild-type genotypes were used (Columbia and Ler) and their mutants (esk-1 and frs-1, respectively), which differ in their freezing resistance. This study's results indicated that the mutant esk-1, described as a freezing-tolerant species showed freezing tolerance only after a cold-acclimation period. The mutant frs-1, described as freezing sensitive, presented freezing avoidance. Both wild genotypes presented LT50 similar to or higher than the ice-nucleation temperature. Thus, the main freezing-resistance mechanism for A. thaliana is avoidance of freezing by supercooling. No injury of the photosynthetic apparatus was shown by measuring the maximal photochemical efficiency (Fv/Fm) and pigments (chlorophyll and carotenoid) during cold acclimation in all genotypes. During cold acclimation, Columbia and esk-1 increased total soluble carbohydrates in leaves. esk-1 was the only genotype that presented freezing tolerance after cold acclimation. This feature could be related to an increase in sugar accumulation in the apoplast.

Light regulation of sucrose-phosphate synthase activity in the freezing-tolerant grass Deschampsia antarctica.

Deschampsia antarctica, a freezing-tolerant grass that has colonized the Maritime Antarctic, has an unusually high content of sucrose (Suc) in leaves, reaching up to 36% of dry weight. Suc accumulation has often been linked with increased activity of sucrose phosphate synthase (SPS; EC: 2.4.1.1.14). SPS, a key enzyme in sucrose biosynthesis, is controlled by an intricate hierarchy of regulatory mechanisms including allosteric modulators, reversible covalent modification in response to illumination, and transcriptional regulation. We hypothesized that during long day conditions in the Antarctic summer D. antarctica can maintain high SPS activity longer by indirect light regulation, thereby leading to a high sucrose accumulation in the leaves. The objectives of this study were to investigate a possible indirect light regulation of SPS activity and the effect of cold and day length on transcriptional and protein level of SPS in D. antarctica. Although SPS activity did not display an endogenous rhythm of activity in continuous light, activation of SPS at the end of the dark period was observed in D. antarctica. This activation of SPS is possibly controlled by covalent modification, because it was inhibited by okadaic acid while the SPS protein level did not significantly change. The highest SPS activity increase was observed after 21 days of cold-acclimation under long day conditions. This increased activity was not related to an increase in SPS gene expression or protein content. High SPS activity in cold long days leading to hyper accumulation of Suc appears to be among the features that permit D. antarctica to survive in the harsh Antarctic conditions.