Dynamics in plant roots and shoots minimize stress, save energy and maintain water and nutrient uptake

Arsova, Borjana; Foster, Kylie J.; Shelden, Megan C.; Bramley, Helen; Watt, Michelle

doi:10.1111/nph.15955

Cited by 47 publications

(38 citation statements)

References 76 publications

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“…When plants are able to use inorganic ions instead of photosynthetic products for osmotic adjustment, the energetic cost of salt tolerance is minimized (Arsova et al ., ). Osmoregulation mechanisms allow salt‐resilient plants to regulate internal water potential thorough ions (or water) movement across plant compartments more effectively than salt‐sensitive species (Perri et al ., 2018a).…”

Section: Discussionmentioning

confidence: 99%

Xylem–phloem hydraulic coupling explains multiple osmoregulatory responses to salt stress

2019

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Summary Salinity is known to affect plant productivity by limiting leaf‐level carbon exchange, root water uptake, and carbohydrates transport in the phloem. However, the mechanisms through which plants respond to salt exposure by adjusting leaf gas exchange and xylem–phloem flow are still mostly unexplored. A physically based model coupling xylem, leaf, and phloem flows is here developed to explain different osmoregulation patterns across species. Hydraulic coupling is controlled by leaf water potential, ψl, and determined under four different maximization hypotheses: water uptake (1), carbon assimilation (2), sucrose transport (3), or (4) profit function – i.e. carbon gain minus hydraulic risk. All four hypotheses assume that finite transpiration occurs, providing a further constraint on ψl. With increasing salinity, the model captures different transpiration patterns observed in halophytes (nonmonotonic) and glycophytes (monotonically decreasing) by reproducing the species‐specific strength of xylem–leaf–phloem coupling. Salt tolerance thus emerges as plant's capability of differentiating between salt‐ and drought‐induced hydraulic risk, and to regulate internal flows and osmolytes accordingly. Results are shown to be consistent across optimization schemes (1–3) for both halophytes and glycophytes. In halophytes, however, profit‐maximization (4) predicts systematically higher ψl than (1–3), pointing to the need of an updated definition of hydraulic cost for halophytes under saline conditions.

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Section: Discussionmentioning

confidence: 99%

Xylem–phloem hydraulic coupling explains multiple osmoregulatory responses to salt stress

2019

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“…The diurnal pattern of transport is an effect that has not previously been described experimentally, however has been hypothesized recently (Arsova et al, 2020). Future work is required to determine whether this fundamental sodium transport characteristic has important implications for how plants survive under conditions of elevated soil sodium conditions.…”

Section: Discussionmentioning

confidence: 96%

Continuous monitoring of plant sodium transport dynamics using clinical PET

Ruwanpathirana

Plett

Williams

et al. 2020

Preprint

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BackgroundThe absorption, translocation, accumulation and excretion of substances are fundamental processes in all organisms including plants, and have been successfully studied using radiotracers labelled with and since 1939. Sodium is one of the most damaging ions to the growth and productivity of crops. Due to the significance of understanding sodium transport in plants, a significant number of studies have been carried out to examine sodium influx, compartmentation, and efflux using - or 24Na-labeled salts. Notably, however, most of these studies employed destructive methods, which has limited our understanding of sodium flux and distribution characteristics in real time, in live plants.Positron emission tomography (PET) has been used successfully in medical research and diagnosis for decades. Due to its ability to visualise and assess physiological and metabolic function, PET imaging has also begun to be employed in plant research. Here, we report the use of a clinical PET scanner with a tracer to examine -influx dynamics in barley plants (Hordeum vulgare L. spp. vulgare – cultivar Bass) under variable nutrient levels, alterations in the day/night light cycle, and the presence of sodium channel inhibitors.Results3D dynamic PET images of whole plants show readily visible translocation from roots to shoots in each examined plant, with rates influenced by both nutrient status and channel inhibition. PET images show that plants cultivated in low-nutrient media transport more than plants cultivated in high-nutrient media, and that uptake is suppressed in the presence of a cation-channel inhibitor. A distinct diurnal pattern of influx was discernible in curves displaying rates of change of relative radioactivity. Plants were found to absorb significantly more during the light period, and anticipate the change in the light/dark cycle by adjusting the sodium influx rate downward in the dark period, an effect not previously described experimentally.ConclusionsWe demonstrate the utility of clinical PET/CT scanners for real-time monitoring of the temporal dynamics of sodium transport in plants. The effects of nutrient deprivation and of ion channel inhibition on sodium influx into barley plants are shown in two proof-of-concept experiments, along with the first-ever 3D-imaging of the light and dark sodium uptake cycles in plants. This method carries significant potential for plant biology research and, in particular, in the context of genetic and treatment effects on sodium acquisition and toxicity in plants.*The authors contributed equally

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“…Alternatively, increased root branching (resulting in greater fine root mass fraction) has been suggested to reduce the energetic cost of Na exclusion (Zolla et al, 2010; Munns et al, 2020a)). Notably, this could come at the cost of reduced water uptake during the day (Arsova et al, 2019), suggesting a possible interaction between the osmotic and ionic components of salt stress through root branching. Greater chlorophyll content as measured could be the result of more chlorophyll per area or thicker leaves.…”

Section: Discussionmentioning

confidence: 99%

Key traits and genes associate with salinity tolerance independent from vigor in cultivated sunflower (Helianthus annuusL.)

Temme

Kerr

Masalia

et al. 2020

Preprint

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With rising food demands, crop production on salinized lands is increasingly necessary. Sunflower, a moderately salt tolerant crop, exhibits a trade-off where more vigorous, high-performing genotypes have a greater proportional decline in biomass under salinity stress. Prior research has found deviations from this relationship across genotypes; the magnitude and direction of these deviations provides a useful metric of tolerance. Here, we identified the traits and genomic regions underlying variation in this expectation-deviation tolerance. We grew a diversity panel under control and salt-stressed conditions and measured a suite of morphological (growth, allocation, plant and leaf morphology) and leaf ionomic traits. The genetic basis of variation in these traits and their plasticity was investigated via genome-wide association studies, which also enabled the identification of genomic regions (i.e., haplotypic blocks) influencing multiple traits. We found that the magnitude of plasticity in whole root mass fraction, fine root mass fraction, and chlorophyll content, as well as leaf Na and K content under saline conditions, were the traits most strongly correlated with expectation-deviation tolerance. Additionally, we identified multiple genomic regions underlying these traits as well as a single gene directly associated with this tolerance metric. Our results show that, by taking the vigor-salinity effect trade-off into account, we can identify unique traits and genes associated with salinity tolerance. Since these traits and genomic regions are distinct from those associated with high vigor (i.e., growth in benign conditions), they provide an avenue for increasing salinity tolerance in high-performing sunflower genotypes without compromising vigor.Single sentence summaryDespite a trade-off between vigor and salinity-induced decline in biomass, distinct traits and genomic regions exist that could modulate this trade-off in cultivated sunflower.

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Dynamics in plant roots and shoots minimize stress, save energy and maintain water and nutrient uptake

Cited by 47 publications

References 76 publications

Xylem–phloem hydraulic coupling explains multiple osmoregulatory responses to salt stress

Xylem–phloem hydraulic coupling explains multiple osmoregulatory responses to salt stress

Continuous monitoring of plant sodium transport dynamics using clinical PET

Key traits and genes associate with salinity tolerance independent from vigor in cultivated sunflower (Helianthus annuusL.)

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