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Climate change and catastrophic events have contributed to rice shortages in several regions due to decreased water availability and soil salinization. Although not adapted to salt or drought stress, two commercial rice varieties achieved tolerance to these stresses by colonizing them with Class 2 fungal endophytes isolated from plants growing across moisture and salinity gradients. Plant growth and development, water usage, ROS sensitivity and osmolytes were measured with and without stress under controlled conditions. The endophytes conferred salt, drought and cold tolerance to growth chamber and greenhouse grown plants.
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Climate change and catastrophic events have contributed to rice shortages in several regions due to decreased water availability and soil salinization. Although not adapted to salt or drought stress, two commercial rice varieties achieved tolerance to these stresses by colonizing them with Class 2 fungal endophytes isolated from plants growing across moisture and salinity gradients.
Plant growth and development, water usage, ROS sensitivity and osmolytes were measured with and without stress under controlled conditions. The endophytes conferred salt, drought and cold tolerance to growth chamber and greenhouse grown plants. These findings indicate that rice plants can exhibit enhanced stress tolerance via symbiosis with Class 2 endophytes, and suggest that symbiotic technology may be useful in mitigating impacts of climate change on other crops and expanding agricultural production onto marginal lands.
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The work is made available under the Creative Commons CC0 public domain dedication. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. She declares this ownership, and states that there was no involvement of AST in the work presented in this manuscript in regards to consultancy, patents, products in development conducted. The studies presented involved only those affiliations listed on the front page of the manuscript.
There has been no marketing of any of the components of the study. She confirms that these studies conducted were in adherence to all the PLoS ONE policies on sharing data and materials. The geographic distribution pattern of plants is thought to be based on climatic and edaphic heterogeneity that occurs across complex habitats  ,  , . All plants express some level of phenotypic plasticity  enabling them to grow in diverse habitats and across environmental gradients  ,  ,  ,  , .
Phenotypic plasticity is defined as the production of multiple phenotypes from a single genotype, depending on environmental conditions and is considered adaptive if it is maintained by natural selection  ,  , .
Plant adaptation to high stress habitats likely involves a combination of phenotypic plasticity and genetic adaptation, and is thought to involve processes exclusive to the plant genome  ,  ,  , . However, the mechanisms responsible for adaptation to high stress habitats are poorly defined. For example, all plants are known to perceive, transmit signals and respond to abiotic stresses such as drought, heat, and salinity  , .
Yet, few species are able to colonize high stress habitats which typically have decreased levels of plant abundance compared to adjacent low stress habitats  , . Although there are numerous reports on the genetic, molecular and physiological bases of how plants respond to stress, the nature of plant adaptation to high stress habitats remains unresolved  ,  , .
However, most ecological studies fail to consider the fact that all plants in natural ecosystems are thought to be symbiotic with fungal endophytes and these endophytes can have profound effects on plant stress tolerance and fitness  , . For example, fungal endophytes can confer fitness benefits to plants including increased root and shoot biomass, increased yield, tolerance to abiotic stresses such as heat, salt, and drought, and to biotic stresses such as pathogens and herbivores  ,  ,  ,  ,  ,  ,  , .
One group of fungal endophytes [Class 2;  ] confer habitat-specific stress tolerance to plants through a process defined as Habitat Adapted Symbiosis . Remarkably, Class 2 endophytes, are capable of colonizing and conferring habitat-specific stress tolerance to monocot and eudicot plants which may suggest that the symbiotic communication responsible for stress tolerance may predate the divergence of these lineages est. During the last several decades, there have been major climatic events that decreased agricultural productivity of rice one of the four major food crops at locations around the world.
For example, in , an earthquake generated tidal wave flooded Indonesia  , and in , a cyclone resulted in a tidal surge that flooded southern Burma. Both of these events resulted in inundation of productive agricultural lands with salt water that decreased or eliminated production of rice for one or more years. During the last 40 years of climate change, increased minimum air temperatures during growing seasons have resulted in a substantial decrease in rice yields in China and the Philippines and are predicted to continue  , .
Collectively, these events along with increasing world-population, have contributed to shortages and increased prices of rice exacerbating hunger and famine issues globally. Climate change has also begun to alter the phenology of currently used commercial rice varieties making predictions about rice availability and abundance less reliable.
Although it may be possible to compensate for some impacts of phenology shifts by incorporating earlier season varieties into agricultural practices  , the adaptive capabilities of rice will ultimately determine the severity of climate change on annual crop yields. However, the adaptive potential of most plants, including rice, is not well characterized. Here we report that the ability of rice to rapidly exhibit stress tolerance is dependent on associations with Class 2 fungal endophytes.
The influence of three endophytes on the ability of rice to tolerate low temperatures, high salinity and desiccation was tested. In addition, the influence of the endophytes on growth, development and water usage was assessed under greenhouse and laboratory conditions. The potential for using symbiotic technologies to mitigate the impacts of climate change is discussed. Both Fusarium culmorum isolate FcRed1 SaltSym and Curvularia protuberata isolate CpD TempSym1 Table 1 significantly increased the growth and development of seedlings in the absence of stress compared to nonsymbioitic plants Fig.
Statistical analysis was performed using Duncan's multiple-range test. Values with the same letters are not significantly different. Each assay was repeated three times. Sterilized, imbibed rice seeds were inoculated with fungal spore solutions S or mock-inoculated NS for 48 hours on water agar plates until seed germination occurred. Symbiotically induced seedling developmental rates Fig.
Differences in growth and root development of S and NS plants were observed using time-lapse photography under 14 hr light cycles Fig. Germinated seedlings were than embedded in the silica sand layer on top of the time-lapse apparatus see Materials and Methods. NS plant shoot growth began before root growth initiated while S plants increased root mass prior to substantial shoot growth. By the time S plants began developing root hairs day 6 , NS plants had not yet begun significant root growth.
While all plants bent over with age, unstressed controls and salt exposed S plants remained hydrated while the NS plants wilted. The remaining plants were not watered for 15,12, 9,7, 5, and 3 days. Post drought stress, plants were re-hydrated for 2 days and viability assessed. Stress treatments began after 2 months and plants were exposed to mM NaCl for 3 weeks, then increased mM NaCl for an additional 3 weeks, and then increased and maintained at mM NaCl until the completion of the study 5 months total.
The colorimetric assay detects indole compounds, some of which are important in promoting plant growth . This assay was specific enough to detect Indoles and not tryptophan. Endophytes were grown in liquid media for 21 days Table 2. Endophytes grown in Mathur's Media with the addition of Trp produced — ppm IAA within 5 days, and levels were maintained until the last time point taken after 21 days.
These results suggest that the growth response in symbiotic plants may be due to endophyte production of IAA or IAA like plant growth stimulating compounds, which can be induced in the presence of Trp, and possibly suppressed by media components e. Additional analysis revealed that IAA was not detected in five-day old S and NS rice seedlings irrespective of a significant growth response in S plants Table 2. The absence of detectible levels of IAA in symbiotic rice seedlings may reflect levels of IAA below detectable range for the assay, the physiological status of plants at the time of analysis, or lack of sufficient Trp for fungal biosynthesis.
Regardless, these results suggest that the potential role of endophytes and IAA production in planta needs to be addressed in greater detail. The ability of habitat-adapted endophytes to confer significant levels of stress tolerance to young rice plants was assessed in double-decker Magenta boxes  under laboratory conditions.
As anticipated, SaltSym conferred significant levels of salt tolerance to rice allowing them to grow at mM NaCl Fig. Rice plants were grown for five weeks without stress before continual exposure to NaCl for three weeks.
To determine the impact of salt stress on mature plants plants taken to seed set , SaltSym and NS plants were grown under greenhouse conditions, without salt stress for two months, and then gradually exposing plants to increasing levels of salt from mM— mM NaCl prior to seed production. Seed production was measured after 5 months of growth, of which, approximately 6 weeks of that time frame, involved exposure to the highest level of salt concentrations of mM NaCl.
Analysis of roots and shoot showed an increase in the root biomass of S plants in the presence and absence of salt stress, and shoot biomass of S plants in the presence and absence of stress, compared to NS plants. These results suggest that through symbiosis, endophytes may play a dual role in growth enhancement and salt stress tolerance. When yields were assessed, a significant difference in seed production was observed in S plants in the presence and absence of stress when compared to NS plants Fig.
Although seed production by S plants was decreased by salt stress, the levels were not significantly different from NS plants grown without stress. Although TempSym1 is adapted to high soil temperatures, the canopy of the plants in which both endophytes were originally isolated, experience below freezing temperatures in the winter and continue to produce vegetative tissues.
All three endophytes TempSym1 and 2, and SaltSym were tested for the degree of drought tolerance they could confer in the absence of any other stress. This was done by determining time-to-wilt after the cessation of watering Fig.
NS plants wilted after 3 days while TempSym1 inoculated plants did not wilt for 9 days. The other two endophytes in this study TempSym2 and SaltSym also conferred drought tolerance 7 and 9 day delay in wilt, respectively, not shown compared to NS plants. Previous studies indicated that these endophytes decrease plant water consumption, which may explain symbiotically conferred drought tolerance .
Two common plant responses to abiotic stresses such as heat, salt and drought involve regulating the levels of osmolytes and reactive oxygen species ROS . Therefore, we analyzed plant osmolyte concentrations and sensitivity to ROS before and after exposure to salt and drought stress Fig.
In the absence of salt stress, S plants had higher levels of osmolytes in shoots compared to NS plants but equivalent levels in the roots. In the presence of salt, all of the plants increased osmolyte levels in both shoots and roots, regardless of the treatment, with SaltSym expressing the highest osmolyte levels.
SaltSym imparts salt tolerance and TempSym1 does not. No significant differences were observed in roots in the absence of salt stress. Time points were chosen when symptoms began to appear wilting and chlorosis in NS stressed plants. Leaf disks were sampled from leaf tissues of similar size, developmental age, and location for optimal side-by-side comparisons. Values indicate the number of leaf disks out of a total of nine that bleached white after exposure to paraquat indicating ROS generation.
Excised leaf discs from plants grown in the absence of stress or exposed to salt and drought stress were analyzed for ROS sensitivity. One way to mimic endogenous production and assess sensitivity to ROS is to expose photosynthetic tissue to the herbicide paraquat, which is reduced by electron transfer from plant photosystem I and oxidized by molecular oxygen resulting in the generation of superoxide ions and subsequent photobleaching .
Leaf discs from plants that were not exposed to stress remained green indicating that ROS was not produced by exposure to paraquat Fig. Rice plants were adapted to cold, salt and drought stress simply by colonization with Class 2 fungal endophytes. Salt and temperature stress tolerance are habitat-adapted traits of the endophytes evaluated in this study . SaltSym, derived from coastal plants Leymus mollis exposed to high salt stress confer salt tolerance, and not temperature tolerance.
The fact that both endophytes conferred cold tolerance may reflect the cold winter temperatures plants experience above ground rather than in the soil. Initial cell signaling and biochemical pathways involved in both hot and cold temperature stress responses begin with the same root physiological processes and later branch off into unique pathways .
To make observations concerning the impacts of cold stress on seedling shoot and root development, rice seeds showing a small white tissue protuberance indicating a high potential success rate of germination were used for the cold stress assays. It is possible that TempSym1 either allows plants to increase metabolic rates at low temperatures or increase metabolic efficiency to overcome affects of low temperature.
Symbiotically induced metabolic efficiency was also observed in laboratory studies showing decreased water consumption and increased biomass in S plants. Salt and drought stress were tested under greenhouse and growth chamber conditions. SaltSym conferred salt tolerance, allowing plants to grow when continually exposed to a solution of mM NaCl Fig.
More importantly, a gradual increase in salt exposure of mature plants effectively eliminated seed production in NS plants. Although mature S plants had reduced seed production under salt stress compared to non-stressed plants, salt stressed S plants produced similar amounts of seed as NS plants grown in the absence of salt stress Fig.
The levels of salt used in these studies are similar to those occurring in agricultural lands after tsunamis or tidal surges . Therefore, we anticipate that using SaltSym may allow growers to mitigate the impacts of salt inundation.
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