The primary symptom of aluminium (Al) toxicity in higher plants is inhibition of root growth. In ... more The primary symptom of aluminium (Al) toxicity in higher plants is inhibition of root growth. In this study, we investigated the spatial sensitivity of maize (Zea mays L.) roots to Al. A divided-chamber technique indicated that only exposure of the terminal 10 to 15 mm of the root to Al resulted in inhibition of growth. Application of Al to all but this apical region of the root had little or no effect on growth for 24 h and caused minimal damage to the root tissue. Small agar blocks infused with Al were then applied to discrete areas of the apex of maize roots to determine which section (root cap, meristem or elongation zone) was more important to Al-induced inhibition of growth. The terminal 20 to 30 mm of root (root cap and meristem) must be exposed to Al for inhibition. Application of Al to the 3-0 mm of root proximal to this terminal zone (elongation zone) resulted in damage to the root tissue but no significant inhibition of growth. Therefore, the visible injuries incurred by roots during Al-stress are not associated directly with the inhibition of root growth. Furthermore, removal of the root cap had no effect on the Al-induced inhibition of root growth in solution experiments and argues against the root cap providing protection from Al stress or serving an essential role in the mechanism of toxicity. We suggest that the meristem is the primary site of Al-toxicity.
The relationship between AI-induced depolarization of root-cell transmembrane electrical potentia... more The relationship between AI-induced depolarization of root-cell transmembrane electrical potentials (E,,,) and AI tolerance in wheat (Triticum aestivum 1.) was investigated. AI exposure induced depolarizations of E,,, in the AI-tolerant wheat cultivars Atlas and ET3, but not in the AI-sensitive wheat cultivars Scout and ES3. l h e depolarizations of E,,, occurred in root cap cells and as far back as 1 O mm from the root tip. l h e depolarization was specific to AI3+; no depolarization was observed when roots were exposed to the rhizotoxic trivalent cation La3+. The AI-induced depolarization occurred in the presence of anion-channel antagonists that blocked the release of malate, indicating that the depolarization is not due to the electrogenic efflux of malate'-. K+-induced depolarizations in the root cap were of the same magnitude as AI-induced depolarizations, but did not trigger malate release, indicating that Alinduced depolarization of root cap cell membrane potentials is probably linked to, but is not sufficient to trigger, malate release. A1 is present in a11 soils, but A1 toxicity is manifested only in acid conditions, in which the phytotoxic form A13+ predominates. The major toxicity symptom observed in plants is inhibition of root growth (Taylor, 1988; Delhaize and Ryan, 1995; Kochian, 1995). Within plant species there is considerable genetic variation in tolerance to Al. In wheat (Tuiticum aestivum L.) Al-tolerant lines tolerate A1 concentrations that are up to 10 times greater than A1 levels that inhibit root growth in Al-sensitive lines (Delhaize and Ryan, 1995). Many Al-tolerant lines of wheat release malate in response to A1 (Delhaize et al., 1993; Basu et al., 1994; Ryan et al., 1995b; Huang et al., 1996), whereas Al-tolerant lines of maize (Zea mays L.) and snapbean (Phaseolus vulgaris L.) release citrate upon exposure to A1 (Miyasaka et al., 1991; Pellet et al., 1995). This exudation of Al-chelating compounds from root tips serves as a mechanism of A1 tolerante by lowering the activity of free A1 in the rhizosphere, and thus excluding A1 from the plant. The level of organic acid exudation is dependent on both the amount of A1 and the duration of exposure. In wheat the rate of malate exudation is constant over time for exposure to a specific level of A1 (Ryan et al., 1995a). When the A1 level is in-This work was supported by U.S. Department of Agriculture/
Copper and iron are essential micronutrients but are toxic when accumulating in cells in excess. ... more Copper and iron are essential micronutrients but are toxic when accumulating in cells in excess. Thus, their uptake by roots is tightly regulated. While plants sense and respond to local copper availability, the systemic regulation of copper uptake has not been documented. By contrast, both local and systemic control for iron uptake has been reported. Iron abundance in the phloem has been suggested to act systemically, regulating the expression of iron uptake genes in the root. Consistently, shoot-to-root iron signaling is disrupted inA. thalianamutants lacking the phloem companion cell-localized iron transporter, AtOPT3:opt3mutants overaccumulate iron in leaves while constitutively upregulating iron deficiency-responsive genes in roots. We report that AtOPT3 transports copper and mediates its delivery from source leaves to sinks including young leaves and developing embryos. Consequently, theopt3mutant accumulates less copper in the phloem, is sensitive to copper deficiency, and mo...
Plant perception of pathogen-associated molecular patterns (PAMPs) and other environmental stress... more Plant perception of pathogen-associated molecular patterns (PAMPs) and other environmental stresses trigger transient ion fluxes at the plasma membrane. Apart from the role of Ca 2+ uptake in signaling, the regulation and significance of PAMPinduced ion fluxes in immunity remain unknown. We characterized the functions of INTEGRIN-LINKED KINASE1 (ILK1) that encodes a Raf-like MAP2K kinase with functions insufficiently understood in plants. Analysis of ILK1 mutants impaired in the expression or kinase activity revealed that ILK1 contributes to plant defense to bacterial pathogens, osmotic stress sensitivity, and cellular responses and total ion accumulation in the plant upon treatment with a bacterial-derived PAMP, flg22. The calmodulin-like protein CML9, a negative modulator of flg22-triggered immunity, interacted with, and suppressed ILK1 kinase activity. ILK1 interacted with and promoted the accumulation of HAK5, a putative (H +)/K + symporter that mediates a high-affinity uptake during K + deficiency. ILK1 or HAK5 expression was required for several flg22 responses including gene induction, growth arrest, and plasma membrane depolarization. Furthermore, flg22 treatment induced a rapid K + efflux at both the plant and cellular levels in wild type, while mutants with impaired ILK1 or HAK5 expression exhibited a comparatively increased K + loss. Taken together, our results position ILK1 as a link between plant defense pathways and K + homeostasis.
There is considerable variability among wheat (Triticum aestivum L.) cultivars in their ability t... more There is considerable variability among wheat (Triticum aestivum L.) cultivars in their ability to grow and yield well in soils that contain very low levels of available Zn. The physiological basis for this tolerance, termed Zn efficiency, is unknown. We investigated the possible role of Zn2+ influx across the root cell plasma membrane in conferring Zn efficiency by measuring short-term 65Zn2+ uptake in two contrasting wheat cultivars, Zn-efficient cv Dagdas and Zn-inefficient cv BDME-10. Plants were grown hydroponically under sufficient and deficient Zn levels, and uptake of 65Zn2+ was measured over a wide range of Zn activities (0.1 nm–80 μm). Under low-Zn conditions, cv BDME-10 displayed more severe Zn deficiency symptoms than cv Dagdas. Uptake experiments revealed the presence of two separate Zn transport systems mediating high- and low-affinity Zn influx. The low-affinity system showed apparent K m values similar to those previously reported for wheat (2–5 μm). Using chelate b...
This report covers the progress during the third year of this project. The state-of-the-art of bi... more This report covers the progress during the third year of this project. The state-of-the-art of biophotolysis was reviewed and a bioengineering analysis carried out. The conclusions were that practical biophotolysis systems are feasible; however, they will require, in most cases, relatively long-term R and D. The biophotolysis system developed under this project, utilizing heterocystous blue-green algae, was demonstrated both indoors and outdoors with a model converter system using the heterocystous blue-grees alga Anabaena cylindrica. Maximal light energy conversion efficiencies were 2.5% indoors and about 0.2% outdoors, averaged for periods of about two weeks. Achievement of such rates required optimization of N/sub 2/ supply and culture density. A small amount of N/sub 2/ in the argon gas phase used to sparge the cultures was beneficial to the stability of a long-term hydrogen-production activity. A relatively small amount of the hydrogen produced by these cultures can be ascribed to the activity of the reversible hydrogenase which was studied by nitrogenase inactivation through poisoning with tungstate. The regulation of nitrogenase activity in these algae was studied through physiological and immunochemical methods. In particular, the oxygen protection mechanism was examined. Thermophilic blue-green algae have potential for biophotolysis; hydrogen production was studied in the laboratory.more » Preliminary experiments on the photofermentation of organic substrates to hydrogen was studied with photosynthetic bacteria.« less
Although citrate transporters are involved in iron (Fe) translocation and aluminum (Al) tolerance... more Although citrate transporters are involved in iron (Fe) translocation and aluminum (Al) tolerance in plants, to date none of them have been shown to confer both biological functions in plant species that utilize Fe-absorption Strategy I. In this study, we demonstrated that AhFRDL1, a citrate transporter gene from peanut (Arachis hypogaea) that is induced by both Fe-deficiency and Al-stress, participates in both root-to-shoot Fe translocation and Al tolerance. Expression of AhFRDL1 induced by Fe deficiency was located in the root stele, but under Al-stress expression was observed across the entire root-tip cross-section. Overexpression of AhFRDL1 restored efficient Fe translocation in Atfrd3 mutants and Al resistance in AtMATE-knockout mutants. Knocking down AhFRDL1 in the roots resulted in reduced xylem citrate and reduced concentrations of active Fe in young leaves. Furthermore, AhFRDL1-knockdown lines had reduced root citrate exudation and were more sensitive to Al toxicity. Compared to an Al-sensitive variety, enhanced AhFRDL1 expression in an Fe-efficient variety contributed to higher levels of Al tolerance and Fe translocation by promoting citrate secretion. These results indicate that AhFRDL1 plays a significant role in Fe translocation and Al tolerance in Fe-efficient peanut varieties under different soil-stress conditions. Given its dual biological functions, AhFRDL1 may serve as a useful genetic marker for breeding for high Fe efficiency and Al tolerance.
Cultures of Anabaena cylindrica, grown on media containing 5 m M N H 4C1 (which represses heteroc... more Cultures of Anabaena cylindrica, grown on media containing 5 m M N H 4C1 (which represses heterocyst formation), evolved hydrogen after a period o f dark incubation under an argon atmosphere. This hydrogen production was not due to nitrogenase activity, which was nearly undetectable, but was due to a hydrogenase. Cultures grown on media with tungsten substituted for molybdenum had a high frequency of heterocysts (15%) and inactive nitrogenase after nitrogen starvation. The hydrogenase activity of these cultures was threefold greater than the activity of non-heterocystous cultures. The effects o f oxygen inhibition on hydrogen evolution by heterocystous cultures suggest that two pools o f hydrogenase activity exist-an oxygen sensitive hydrogen evolution in vegetative cells and a relatively oxygen-resistent hydrogen evolution in heterocysts. In either case, inhibition by oxygen was reversible. Light had an inhibitory effect on net hydrogen evolution. Hydrogen production in vitro was much higher than in vivo, indicating that in vivo hydrogenase activity is limited by endogenous reductant supply.
Background: Proton stress and aluminum (Al) toxicity are major constraints limiting crop growth a... more Background: Proton stress and aluminum (Al) toxicity are major constraints limiting crop growth and yields on acid soils (pH < 5). In Arabidopsis, STOP1 is a master transcription factor that controls the expression of a set of well-characterized Al tolerance genes and unknown processes involved in low pH resistance. As a result, loss-of-function stop1 mutants are extremely sensitive to low pH and Al stresses. Results: Here, we report on screens of an ethyl-methane sulphonate (EMS)-mutagenized stop1 population and isolation of nine strong stop1 suppressor mutants, i.e., the tolerant to proton stress (tps) mutants, with significantly enhanced root growth at low pH (4.3). Genetic analyses indicated these dominant and partial gain-of-function mutants are caused by mutations in single nuclear genes outside the STOP1 locus. Physiological characterization of the responses of these tps mutants to excess levels of Al and other metal ions further classified them into five groups. Three tps mutants also displayed enhanced resistance to Al stress, indicating that these tps mutations partially rescue the hypersensitive phenotypes of stop1 to both low pH stress and Al stress. The other six tps mutants showed enhanced resistance only to low pH stress but not to Al stress. We carried out further physiologic and mapping-by-sequencing analyses for two tps mutants with enhanced resistance to both low pH and Al stresses and identified the genomic regions and candidate loci in chromosomes 1 and 2 that harbor these two TPS genes. Conclusion: We have identified and characterized nine strong stop1 suppressor mutants. Candidate loci for two tps mutations that partially rescue the hypersensitive phenotypes of stop1 to low pH and Al stresses were identified by mapping-by-sequencing approaches. Further studies could provide insights into the structure and function of TPSs and the regulatory networks underlying the STOP1-mediated processes that lead to resistance to low pH and Al stresses in Arabidopsis.
Key message Association analysis for ionomic concentrations of 20 elements identified independent... more Key message Association analysis for ionomic concentrations of 20 elements identified independent genetic factors underlying the root and shoot ionomes of rice, providing a platform for selecting and dissecting causal genetic variants. Abstract Understanding the genetic basis of mineral nutrient acquisition is key to fully describing how terrestrial organisms interact with the non-living environment. Rice (Oryza sativa L.) serves both as a model organism for genetic studies and as an important component of the global food system. Studies in rice ionomics have primarily focused on above ground tissues evaluated from field-grown plants. Here, we describe a comprehensive study of the genetic basis of the rice ionome in both roots and shoots of 6-week-old rice plants for 20 elements using a controlled hydroponics growth system. Building on the wealth of publicly available rice genomic resources, including a panel of 373 diverse rice lines, 4.8 M genome-wide single-nucleotide polymorphis...
Crop tolerance to multiple abiotic stresses has long been pursued as a Holy Grail in plant breedi... more Crop tolerance to multiple abiotic stresses has long been pursued as a Holy Grail in plant breeding efforts that target crop adaptation to tropical soils. On tropical, acidic soils, aluminum (Al) toxicity, low phosphorus (P) availability and drought stress are the major limitations to yield stability. Molecular breeding based on a small suite of pleiotropic genes, particularly those with moderate to major phenotypic effects, could help circumvent the need for complex breeding designs and large population sizes aimed at selecting transgressive progeny accumulating favorable alleles controlling polygenic traits. The underlying question is twofold: do common tolerance mechanisms to Al toxicity, P deficiency and drought exist? And if they do, will they be useful in a plant breeding program that targets stress-prone environments. The selective environments in tropical regions are such that multiple, co-existing regulatory networks may drive the fixation of either distinctly different or a smaller number of pleiotropic abiotic stress tolerance genes. Recent studies suggest that genes contributing to crop adaptation to acidic soils, such as the major Arabidopsis Al tolerance protein, AtALMT1, which encodes an aluminum-activated root malate transporter, may influence both Al tolerance and P acquisition via changes in root system morphology and architecture. However, transacting elements such as transcription factors (TFs) may be the best option for pleiotropic control of multiple abiotic stress genes, due to their small and often multiple binding sequences in the genome. One such example is the C2H2-type zinc finger, AtSTOP1, which is a transcriptional regulator of a number of Arabidopsis Al tolerance genes, including AtMATE and AtALMT1, and has been shown to activate AtALMT1, not only in response to Al but also low soil P. The large WRKY family of transcription factors are also known to affect a broad spectrum of phenotypes, some of which are related to acidic soil abiotic stress responses. Hence, we focus here on signaling proteins such as TFs and protein kinases to identify, from the literature, evidence for
Key message A multiparental random mating population used in sorghum breeding is amenable for the... more Key message A multiparental random mating population used in sorghum breeding is amenable for the detection of QTLs related to tropical soil adaptation, fine mapping of underlying genes and genomic selection approaches. Abstract Tropical soils where low phosphorus (P) and aluminum (Al) toxicity limit sorghum [Sorghum bicolor (L.) Moench] production are widespread in the developing world. We report on BRP13R, a multiparental random mating population (MP-RMP), which is commonly used in sorghum recurrent selection targeting tropical soil adaptation. Recombination dissipated much of BRP13R's likely original population structure and average linkage disequilibrium (LD) persisted up to 2.5 Mb, establishing BRP13R as a middle ground between biparental populations and sorghum association panels. Genome-wide association mapping (GWAS) identified conserved QTL from previous studies, such as for root morphology and grain yield under low-P, and indicated the importance of dominance in the genetic architecture of grain yield. By overlapping consensus QTL regions, we mapped two candidate P efficiency genes to a ~ 5 Mb region on chromosomes 6 (ALMT) and 9 (PHO2). Remarkably, we find that only 200 progeny genotyped with ~ 45,000 markers in BRP13R can lead to GWAS-based positional cloning of naturally rare, subpopulation-specific alleles, such as for SbMATE-conditioned Al tolerance. Genomic selection was found to be useful in such MP-RMP, particularly if markers in LD with major genes are fitted as fixed effects into GBLUP models accommodating dominance. Shifts in allele frequencies in progeny contrasting for grain yield indicated that intermediate to minor-effect genes on P efficiency, such as SbPSTOL1 genes, can be employed in pre-breeding via allele mining in the base population. Therefore, MP-RMPs such as BRP13R emerge as multipurpose resources for efficient gene discovery and deployment for breeding sorghum cultivars adapted to tropical soils. Communicated by Hai-Chun Jing.
Aluminum (Al) toxicity on acidic soils significantly damages plant roots and inhibits root growth... more Aluminum (Al) toxicity on acidic soils significantly damages plant roots and inhibits root growth. Hence, crops intoxicated by Al become more sensitive to drought stress and mineral nutrient deficiencies, particularly phosphorus (P) deficiency, which is highly unavailable on tropical soils. Advances in our understanding of the physiological and genetic mechanisms that govern plant Al resistance have led to the identification of Al resistance genes, both in model systems and in crop species. It has long been known that Al resistance has a beneficial effect on crop adaptation to acidic soils. This positive effect happens because the root systems of Al resistant plants show better development in the presence of soil ionic Al 3+ and are, consequently, more efficient in absorbing subsoil water and mineral nutrients. This effect of Al resistance on crop production, by itself, warrants intensified efforts to develop and implement, on a breeding scale, modern selection strategies to profit from the knowledge of the molecular determinants of plant Al resistance. Recent studies now suggest that Al resistance can exert pleiotropic effects on P acquisition, potentially expanding the role of Al resistance on crop adaptation to acidic soils. This appears to occur via both organic acid (OA)-and non-OA transporters governing a joint, iron-dependent interplay between Al resistance and enhanced P uptake, via changes in root system architecture. Current research suggests this interplay to be part of a P stress response, suggesting that this mechanism could have evolved in crop species to improve adaptation to acidic soils. Should this pleiotropism prove functional in crop species grown on acidic soils, molecular breeding based on Al resistance genes may have a much broader impact on crop performance than previously anticipated. To explore this possibility, here we review the components of this putative effect of Al resistance genes on P stress responses and P nutrition to provide the foundation necessary to discuss the recent evidence suggesting pleiotropy as a genetic linkage between Al resistance and P efficiency. We conclude by exploring what may be needed to enhance the utilization of Al resistance genes to improve crop production on acidic soils.
ABSTRACTTranscription factors (TFs) mediate stress resistance indirectly via physiological mechan... more ABSTRACTTranscription factors (TFs) mediate stress resistance indirectly via physiological mechanisms driven by the genes they regulate. When studying TF-mediated stress resistance, it is important to understand how TFs interact with different genetic backgrounds. Here, we fine-mapped the aluminum (Al) resistance QTL Alt12.1 to a 44 Kb region containing six gene models. Among them is ART1, which encodes a C2H2-type zinc finger TF required for Al resistance in rice. The parents of the mapping population, Al-resistant Azucena (tropical japonica) and Al-sensitive IR64 (indica), showed similar ART1 expression levels but extensive sequence polymorphism within the ART1 coding region. Using reciprocal near-isogenic lines (NILs) in the Azucena and IR64 genetic backgrounds, we examined how allele-swapping Alt12.1 would affect plant responses to Al. Analysis of global transcriptional responses to Al stress in roots of the NILs alongside their recurrent parents demonstrated that the ART1 from ...
The role of AI interactions with root-cell plasma memhrane (PM) Ca2+ channels in AI toxicity and ... more The role of AI interactions with root-cell plasma memhrane (PM) Ca2+ channels in AI toxicity and resistance was studied. l h e experimental approach involved the imposition of a transmembrane electrical potential (via K+ diffusion) in right-side-out PM vesicles derived from roots of two wheat (Trificum aestivum L.) cultivars (AI-sensitive Scout 66 and AI-resistant Atlas 66). W e previously used this technique to characterize a voltage-dependent Ca" channel in the wheat root PM (J.W. Huang, D.L. Crunes, L.V. Kochian 119941 Proc Natl Acad Sci USA 91: 3473-3477). W e found that AI3+ effectively blocked this P M Cazf channel; however, AI3+ blocked this Ca2+ channel equally well in both the AI-sensitive and-resistant cultivars. I t was found that the differential genotypic sensitivity of this Ca2+ transport system to AI in intact roots versus isolated PM vesicles was due to AI-induced malate exudation localized to the root apex in AI-resistant Atlas but not in AI-sensitive Scout. Because malate can effectively chelate AI3+ in the rhizosphere and exclude it from the root apex, the differential sensitivity of Ca2+ influx to AI in intact roots of AI-resistant versus AI-sensitive wheat cultivars is probahly dueto the maintenance of lower AI3+ activities in the root apical rhizosphere of the resistant cultivar. A1 toxicity is the primary environmental stress limiting crop productivity on acid soils. One of the proposed mechanisms of A1 toxicity involves A1 interaction with ion transport systems functioning at the root-cell PM (Taylor, 1988; Kochian, 1995). The role of A1/Ca2+ transport interactions in the mechanisms of A1 toxicity has recently received considerable attention, because Ca2+ plays a central role in the regulation of many plant cellular processes, including mitosis and cytokinesis, gravitropism, polar growth, and cytoplasmic streaming (Williamson and Ashley, 1982; Hepler and Wayne, 1985). A1 inhibition of Ca2+ influx into plant cells is rapid and reversible, and the A1 blockage of Caz+ influx precedes visible symptoms of A1 toxicity
Proceedings of the National Academy of Sciences of the United States of America, Jan 24, 2017
Members of the aquaporin (AQP) family have been suggested to transport aluminum (Al) in plants; h... more Members of the aquaporin (AQP) family have been suggested to transport aluminum (Al) in plants; however, the Al form transported by AQPs and the roles of AQPs in Al tolerance remain elusive. Here we report that NIP1;2, a plasma membrane-localized member of the Arabidopsis nodulin 26-like intrinsic protein (NIP) subfamily of the AQP family, facilitates Al-malate transport from the root cell wall into the root symplasm, with subsequent Al xylem loading and root-to-shoot translocation, which are critical steps in an internal Al tolerance mechanism in Arabidopsis We found that NIP1;2 transcripts are expressed mainly in the root tips, and that this expression is enhanced by Al but not by other metal stresses. Mutations in NIP1;2 lead to hyperaccumulation of toxic Al(3+) in the root cell wall, inhibition of root-to-shoot Al translocation, and a significant reduction in Al tolerance. NIP1;2 facilitates the transport of Al-malate, but not Al(3+) ions, in both yeast and Arabidopsis We demons...
Radiotracer techniques were employed to characterize 65Zn2+ influx into the root symplasm and tra... more Radiotracer techniques were employed to characterize 65Zn2+ influx into the root symplasm and translocation to the shoot in Thlaspi caerulescens, a Zn hyperaccumulator, and Thlaspi arvense, a nonaccumulator. A protocol was developed that allowed us to quantify unidirectional 65Zn2+ influx across the root-cell plasma membrane (20 min of radioactive uptake followed by 15 min of desorption in a 100 [mu]M ZnCl2 + 5 mM CaCl2 solution). Concentration-dependent Zn2+ influx in both Thlaspi species yielded nonsaturating kinetic curves that could be resolved into linear and saturable components. The linear kinetic component was shown to be cell-wall-bound Zn2+ remaining in the root after desorption, and the saturable component was due to Zn2+ influx across the root-cell plasma membrane. This saturable component followed Michaelis-Menten kinetics, with similar apparent Michaelis constant values for T. caerulescens and T. arvense (8 and 6 [mu]M, respectively). However, the maximum initial veloc...
The relationship between Al-induced depolarization of root-cell transmembrane electrical potentia... more The relationship between Al-induced depolarization of root-cell transmembrane electrical potentials (Em) and Al tolerance in wheat (Triticum aestivum L.) was investigated. Al exposure induced depolarizations of Em in the Al-tolerant wheat cultivars Atlas and ET3, but not in the Al-sensitive wheat cultivars Scout and ES3. The depolarizations of Em occured in root cap cells and as far back as 10 mm from the root tip. The depolarization was specific to Al3+; no depolarization was observed when roots were exposed to the rhizotoxic trivalent cation La3+. The Al-induced depolarization occurred in the presence of anion-channel antagonists that blocked the release of malate, indicating that the depolarization is not due to the electrogenic efflux of malate2-. K+-induced depolarizations in the root cap were of the same magnitude as Al-induced depolarizations, but did not trigger malate release, indicating that Al-induced depolarization of root cap cell membrane potentials is probably linked ...
Many plant biologists work on the identification of genes related to abiotic stress resistance, b... more Many plant biologists work on the identification of genes related to abiotic stress resistance, but the term 'stress resistance gene' is widely used without proper definition. Here it is argued that there is a need to update our understanding of this term and for standardization to facilitate integration of research data.
The primary symptom of aluminium (Al) toxicity in higher plants is inhibition of root growth. In ... more The primary symptom of aluminium (Al) toxicity in higher plants is inhibition of root growth. In this study, we investigated the spatial sensitivity of maize (Zea mays L.) roots to Al. A divided-chamber technique indicated that only exposure of the terminal 10 to 15 mm of the root to Al resulted in inhibition of growth. Application of Al to all but this apical region of the root had little or no effect on growth for 24 h and caused minimal damage to the root tissue. Small agar blocks infused with Al were then applied to discrete areas of the apex of maize roots to determine which section (root cap, meristem or elongation zone) was more important to Al-induced inhibition of growth. The terminal 20 to 30 mm of root (root cap and meristem) must be exposed to Al for inhibition. Application of Al to the 3-0 mm of root proximal to this terminal zone (elongation zone) resulted in damage to the root tissue but no significant inhibition of growth. Therefore, the visible injuries incurred by roots during Al-stress are not associated directly with the inhibition of root growth. Furthermore, removal of the root cap had no effect on the Al-induced inhibition of root growth in solution experiments and argues against the root cap providing protection from Al stress or serving an essential role in the mechanism of toxicity. We suggest that the meristem is the primary site of Al-toxicity.
The relationship between AI-induced depolarization of root-cell transmembrane electrical potentia... more The relationship between AI-induced depolarization of root-cell transmembrane electrical potentials (E,,,) and AI tolerance in wheat (Triticum aestivum 1.) was investigated. AI exposure induced depolarizations of E,,, in the AI-tolerant wheat cultivars Atlas and ET3, but not in the AI-sensitive wheat cultivars Scout and ES3. l h e depolarizations of E,,, occurred in root cap cells and as far back as 1 O mm from the root tip. l h e depolarization was specific to AI3+; no depolarization was observed when roots were exposed to the rhizotoxic trivalent cation La3+. The AI-induced depolarization occurred in the presence of anion-channel antagonists that blocked the release of malate, indicating that the depolarization is not due to the electrogenic efflux of malate'-. K+-induced depolarizations in the root cap were of the same magnitude as AI-induced depolarizations, but did not trigger malate release, indicating that Alinduced depolarization of root cap cell membrane potentials is probably linked to, but is not sufficient to trigger, malate release. A1 is present in a11 soils, but A1 toxicity is manifested only in acid conditions, in which the phytotoxic form A13+ predominates. The major toxicity symptom observed in plants is inhibition of root growth (Taylor, 1988; Delhaize and Ryan, 1995; Kochian, 1995). Within plant species there is considerable genetic variation in tolerance to Al. In wheat (Tuiticum aestivum L.) Al-tolerant lines tolerate A1 concentrations that are up to 10 times greater than A1 levels that inhibit root growth in Al-sensitive lines (Delhaize and Ryan, 1995). Many Al-tolerant lines of wheat release malate in response to A1 (Delhaize et al., 1993; Basu et al., 1994; Ryan et al., 1995b; Huang et al., 1996), whereas Al-tolerant lines of maize (Zea mays L.) and snapbean (Phaseolus vulgaris L.) release citrate upon exposure to A1 (Miyasaka et al., 1991; Pellet et al., 1995). This exudation of Al-chelating compounds from root tips serves as a mechanism of A1 tolerante by lowering the activity of free A1 in the rhizosphere, and thus excluding A1 from the plant. The level of organic acid exudation is dependent on both the amount of A1 and the duration of exposure. In wheat the rate of malate exudation is constant over time for exposure to a specific level of A1 (Ryan et al., 1995a). When the A1 level is in-This work was supported by U.S. Department of Agriculture/
Copper and iron are essential micronutrients but are toxic when accumulating in cells in excess. ... more Copper and iron are essential micronutrients but are toxic when accumulating in cells in excess. Thus, their uptake by roots is tightly regulated. While plants sense and respond to local copper availability, the systemic regulation of copper uptake has not been documented. By contrast, both local and systemic control for iron uptake has been reported. Iron abundance in the phloem has been suggested to act systemically, regulating the expression of iron uptake genes in the root. Consistently, shoot-to-root iron signaling is disrupted inA. thalianamutants lacking the phloem companion cell-localized iron transporter, AtOPT3:opt3mutants overaccumulate iron in leaves while constitutively upregulating iron deficiency-responsive genes in roots. We report that AtOPT3 transports copper and mediates its delivery from source leaves to sinks including young leaves and developing embryos. Consequently, theopt3mutant accumulates less copper in the phloem, is sensitive to copper deficiency, and mo...
Plant perception of pathogen-associated molecular patterns (PAMPs) and other environmental stress... more Plant perception of pathogen-associated molecular patterns (PAMPs) and other environmental stresses trigger transient ion fluxes at the plasma membrane. Apart from the role of Ca 2+ uptake in signaling, the regulation and significance of PAMPinduced ion fluxes in immunity remain unknown. We characterized the functions of INTEGRIN-LINKED KINASE1 (ILK1) that encodes a Raf-like MAP2K kinase with functions insufficiently understood in plants. Analysis of ILK1 mutants impaired in the expression or kinase activity revealed that ILK1 contributes to plant defense to bacterial pathogens, osmotic stress sensitivity, and cellular responses and total ion accumulation in the plant upon treatment with a bacterial-derived PAMP, flg22. The calmodulin-like protein CML9, a negative modulator of flg22-triggered immunity, interacted with, and suppressed ILK1 kinase activity. ILK1 interacted with and promoted the accumulation of HAK5, a putative (H +)/K + symporter that mediates a high-affinity uptake during K + deficiency. ILK1 or HAK5 expression was required for several flg22 responses including gene induction, growth arrest, and plasma membrane depolarization. Furthermore, flg22 treatment induced a rapid K + efflux at both the plant and cellular levels in wild type, while mutants with impaired ILK1 or HAK5 expression exhibited a comparatively increased K + loss. Taken together, our results position ILK1 as a link between plant defense pathways and K + homeostasis.
There is considerable variability among wheat (Triticum aestivum L.) cultivars in their ability t... more There is considerable variability among wheat (Triticum aestivum L.) cultivars in their ability to grow and yield well in soils that contain very low levels of available Zn. The physiological basis for this tolerance, termed Zn efficiency, is unknown. We investigated the possible role of Zn2+ influx across the root cell plasma membrane in conferring Zn efficiency by measuring short-term 65Zn2+ uptake in two contrasting wheat cultivars, Zn-efficient cv Dagdas and Zn-inefficient cv BDME-10. Plants were grown hydroponically under sufficient and deficient Zn levels, and uptake of 65Zn2+ was measured over a wide range of Zn activities (0.1 nm–80 μm). Under low-Zn conditions, cv BDME-10 displayed more severe Zn deficiency symptoms than cv Dagdas. Uptake experiments revealed the presence of two separate Zn transport systems mediating high- and low-affinity Zn influx. The low-affinity system showed apparent K m values similar to those previously reported for wheat (2–5 μm). Using chelate b...
This report covers the progress during the third year of this project. The state-of-the-art of bi... more This report covers the progress during the third year of this project. The state-of-the-art of biophotolysis was reviewed and a bioengineering analysis carried out. The conclusions were that practical biophotolysis systems are feasible; however, they will require, in most cases, relatively long-term R and D. The biophotolysis system developed under this project, utilizing heterocystous blue-green algae, was demonstrated both indoors and outdoors with a model converter system using the heterocystous blue-grees alga Anabaena cylindrica. Maximal light energy conversion efficiencies were 2.5% indoors and about 0.2% outdoors, averaged for periods of about two weeks. Achievement of such rates required optimization of N/sub 2/ supply and culture density. A small amount of N/sub 2/ in the argon gas phase used to sparge the cultures was beneficial to the stability of a long-term hydrogen-production activity. A relatively small amount of the hydrogen produced by these cultures can be ascribed to the activity of the reversible hydrogenase which was studied by nitrogenase inactivation through poisoning with tungstate. The regulation of nitrogenase activity in these algae was studied through physiological and immunochemical methods. In particular, the oxygen protection mechanism was examined. Thermophilic blue-green algae have potential for biophotolysis; hydrogen production was studied in the laboratory.more » Preliminary experiments on the photofermentation of organic substrates to hydrogen was studied with photosynthetic bacteria.« less
Although citrate transporters are involved in iron (Fe) translocation and aluminum (Al) tolerance... more Although citrate transporters are involved in iron (Fe) translocation and aluminum (Al) tolerance in plants, to date none of them have been shown to confer both biological functions in plant species that utilize Fe-absorption Strategy I. In this study, we demonstrated that AhFRDL1, a citrate transporter gene from peanut (Arachis hypogaea) that is induced by both Fe-deficiency and Al-stress, participates in both root-to-shoot Fe translocation and Al tolerance. Expression of AhFRDL1 induced by Fe deficiency was located in the root stele, but under Al-stress expression was observed across the entire root-tip cross-section. Overexpression of AhFRDL1 restored efficient Fe translocation in Atfrd3 mutants and Al resistance in AtMATE-knockout mutants. Knocking down AhFRDL1 in the roots resulted in reduced xylem citrate and reduced concentrations of active Fe in young leaves. Furthermore, AhFRDL1-knockdown lines had reduced root citrate exudation and were more sensitive to Al toxicity. Compared to an Al-sensitive variety, enhanced AhFRDL1 expression in an Fe-efficient variety contributed to higher levels of Al tolerance and Fe translocation by promoting citrate secretion. These results indicate that AhFRDL1 plays a significant role in Fe translocation and Al tolerance in Fe-efficient peanut varieties under different soil-stress conditions. Given its dual biological functions, AhFRDL1 may serve as a useful genetic marker for breeding for high Fe efficiency and Al tolerance.
Cultures of Anabaena cylindrica, grown on media containing 5 m M N H 4C1 (which represses heteroc... more Cultures of Anabaena cylindrica, grown on media containing 5 m M N H 4C1 (which represses heterocyst formation), evolved hydrogen after a period o f dark incubation under an argon atmosphere. This hydrogen production was not due to nitrogenase activity, which was nearly undetectable, but was due to a hydrogenase. Cultures grown on media with tungsten substituted for molybdenum had a high frequency of heterocysts (15%) and inactive nitrogenase after nitrogen starvation. The hydrogenase activity of these cultures was threefold greater than the activity of non-heterocystous cultures. The effects o f oxygen inhibition on hydrogen evolution by heterocystous cultures suggest that two pools o f hydrogenase activity exist-an oxygen sensitive hydrogen evolution in vegetative cells and a relatively oxygen-resistent hydrogen evolution in heterocysts. In either case, inhibition by oxygen was reversible. Light had an inhibitory effect on net hydrogen evolution. Hydrogen production in vitro was much higher than in vivo, indicating that in vivo hydrogenase activity is limited by endogenous reductant supply.
Background: Proton stress and aluminum (Al) toxicity are major constraints limiting crop growth a... more Background: Proton stress and aluminum (Al) toxicity are major constraints limiting crop growth and yields on acid soils (pH < 5). In Arabidopsis, STOP1 is a master transcription factor that controls the expression of a set of well-characterized Al tolerance genes and unknown processes involved in low pH resistance. As a result, loss-of-function stop1 mutants are extremely sensitive to low pH and Al stresses. Results: Here, we report on screens of an ethyl-methane sulphonate (EMS)-mutagenized stop1 population and isolation of nine strong stop1 suppressor mutants, i.e., the tolerant to proton stress (tps) mutants, with significantly enhanced root growth at low pH (4.3). Genetic analyses indicated these dominant and partial gain-of-function mutants are caused by mutations in single nuclear genes outside the STOP1 locus. Physiological characterization of the responses of these tps mutants to excess levels of Al and other metal ions further classified them into five groups. Three tps mutants also displayed enhanced resistance to Al stress, indicating that these tps mutations partially rescue the hypersensitive phenotypes of stop1 to both low pH stress and Al stress. The other six tps mutants showed enhanced resistance only to low pH stress but not to Al stress. We carried out further physiologic and mapping-by-sequencing analyses for two tps mutants with enhanced resistance to both low pH and Al stresses and identified the genomic regions and candidate loci in chromosomes 1 and 2 that harbor these two TPS genes. Conclusion: We have identified and characterized nine strong stop1 suppressor mutants. Candidate loci for two tps mutations that partially rescue the hypersensitive phenotypes of stop1 to low pH and Al stresses were identified by mapping-by-sequencing approaches. Further studies could provide insights into the structure and function of TPSs and the regulatory networks underlying the STOP1-mediated processes that lead to resistance to low pH and Al stresses in Arabidopsis.
Key message Association analysis for ionomic concentrations of 20 elements identified independent... more Key message Association analysis for ionomic concentrations of 20 elements identified independent genetic factors underlying the root and shoot ionomes of rice, providing a platform for selecting and dissecting causal genetic variants. Abstract Understanding the genetic basis of mineral nutrient acquisition is key to fully describing how terrestrial organisms interact with the non-living environment. Rice (Oryza sativa L.) serves both as a model organism for genetic studies and as an important component of the global food system. Studies in rice ionomics have primarily focused on above ground tissues evaluated from field-grown plants. Here, we describe a comprehensive study of the genetic basis of the rice ionome in both roots and shoots of 6-week-old rice plants for 20 elements using a controlled hydroponics growth system. Building on the wealth of publicly available rice genomic resources, including a panel of 373 diverse rice lines, 4.8 M genome-wide single-nucleotide polymorphis...
Crop tolerance to multiple abiotic stresses has long been pursued as a Holy Grail in plant breedi... more Crop tolerance to multiple abiotic stresses has long been pursued as a Holy Grail in plant breeding efforts that target crop adaptation to tropical soils. On tropical, acidic soils, aluminum (Al) toxicity, low phosphorus (P) availability and drought stress are the major limitations to yield stability. Molecular breeding based on a small suite of pleiotropic genes, particularly those with moderate to major phenotypic effects, could help circumvent the need for complex breeding designs and large population sizes aimed at selecting transgressive progeny accumulating favorable alleles controlling polygenic traits. The underlying question is twofold: do common tolerance mechanisms to Al toxicity, P deficiency and drought exist? And if they do, will they be useful in a plant breeding program that targets stress-prone environments. The selective environments in tropical regions are such that multiple, co-existing regulatory networks may drive the fixation of either distinctly different or a smaller number of pleiotropic abiotic stress tolerance genes. Recent studies suggest that genes contributing to crop adaptation to acidic soils, such as the major Arabidopsis Al tolerance protein, AtALMT1, which encodes an aluminum-activated root malate transporter, may influence both Al tolerance and P acquisition via changes in root system morphology and architecture. However, transacting elements such as transcription factors (TFs) may be the best option for pleiotropic control of multiple abiotic stress genes, due to their small and often multiple binding sequences in the genome. One such example is the C2H2-type zinc finger, AtSTOP1, which is a transcriptional regulator of a number of Arabidopsis Al tolerance genes, including AtMATE and AtALMT1, and has been shown to activate AtALMT1, not only in response to Al but also low soil P. The large WRKY family of transcription factors are also known to affect a broad spectrum of phenotypes, some of which are related to acidic soil abiotic stress responses. Hence, we focus here on signaling proteins such as TFs and protein kinases to identify, from the literature, evidence for
Key message A multiparental random mating population used in sorghum breeding is amenable for the... more Key message A multiparental random mating population used in sorghum breeding is amenable for the detection of QTLs related to tropical soil adaptation, fine mapping of underlying genes and genomic selection approaches. Abstract Tropical soils where low phosphorus (P) and aluminum (Al) toxicity limit sorghum [Sorghum bicolor (L.) Moench] production are widespread in the developing world. We report on BRP13R, a multiparental random mating population (MP-RMP), which is commonly used in sorghum recurrent selection targeting tropical soil adaptation. Recombination dissipated much of BRP13R's likely original population structure and average linkage disequilibrium (LD) persisted up to 2.5 Mb, establishing BRP13R as a middle ground between biparental populations and sorghum association panels. Genome-wide association mapping (GWAS) identified conserved QTL from previous studies, such as for root morphology and grain yield under low-P, and indicated the importance of dominance in the genetic architecture of grain yield. By overlapping consensus QTL regions, we mapped two candidate P efficiency genes to a ~ 5 Mb region on chromosomes 6 (ALMT) and 9 (PHO2). Remarkably, we find that only 200 progeny genotyped with ~ 45,000 markers in BRP13R can lead to GWAS-based positional cloning of naturally rare, subpopulation-specific alleles, such as for SbMATE-conditioned Al tolerance. Genomic selection was found to be useful in such MP-RMP, particularly if markers in LD with major genes are fitted as fixed effects into GBLUP models accommodating dominance. Shifts in allele frequencies in progeny contrasting for grain yield indicated that intermediate to minor-effect genes on P efficiency, such as SbPSTOL1 genes, can be employed in pre-breeding via allele mining in the base population. Therefore, MP-RMPs such as BRP13R emerge as multipurpose resources for efficient gene discovery and deployment for breeding sorghum cultivars adapted to tropical soils. Communicated by Hai-Chun Jing.
Aluminum (Al) toxicity on acidic soils significantly damages plant roots and inhibits root growth... more Aluminum (Al) toxicity on acidic soils significantly damages plant roots and inhibits root growth. Hence, crops intoxicated by Al become more sensitive to drought stress and mineral nutrient deficiencies, particularly phosphorus (P) deficiency, which is highly unavailable on tropical soils. Advances in our understanding of the physiological and genetic mechanisms that govern plant Al resistance have led to the identification of Al resistance genes, both in model systems and in crop species. It has long been known that Al resistance has a beneficial effect on crop adaptation to acidic soils. This positive effect happens because the root systems of Al resistant plants show better development in the presence of soil ionic Al 3+ and are, consequently, more efficient in absorbing subsoil water and mineral nutrients. This effect of Al resistance on crop production, by itself, warrants intensified efforts to develop and implement, on a breeding scale, modern selection strategies to profit from the knowledge of the molecular determinants of plant Al resistance. Recent studies now suggest that Al resistance can exert pleiotropic effects on P acquisition, potentially expanding the role of Al resistance on crop adaptation to acidic soils. This appears to occur via both organic acid (OA)-and non-OA transporters governing a joint, iron-dependent interplay between Al resistance and enhanced P uptake, via changes in root system architecture. Current research suggests this interplay to be part of a P stress response, suggesting that this mechanism could have evolved in crop species to improve adaptation to acidic soils. Should this pleiotropism prove functional in crop species grown on acidic soils, molecular breeding based on Al resistance genes may have a much broader impact on crop performance than previously anticipated. To explore this possibility, here we review the components of this putative effect of Al resistance genes on P stress responses and P nutrition to provide the foundation necessary to discuss the recent evidence suggesting pleiotropy as a genetic linkage between Al resistance and P efficiency. We conclude by exploring what may be needed to enhance the utilization of Al resistance genes to improve crop production on acidic soils.
ABSTRACTTranscription factors (TFs) mediate stress resistance indirectly via physiological mechan... more ABSTRACTTranscription factors (TFs) mediate stress resistance indirectly via physiological mechanisms driven by the genes they regulate. When studying TF-mediated stress resistance, it is important to understand how TFs interact with different genetic backgrounds. Here, we fine-mapped the aluminum (Al) resistance QTL Alt12.1 to a 44 Kb region containing six gene models. Among them is ART1, which encodes a C2H2-type zinc finger TF required for Al resistance in rice. The parents of the mapping population, Al-resistant Azucena (tropical japonica) and Al-sensitive IR64 (indica), showed similar ART1 expression levels but extensive sequence polymorphism within the ART1 coding region. Using reciprocal near-isogenic lines (NILs) in the Azucena and IR64 genetic backgrounds, we examined how allele-swapping Alt12.1 would affect plant responses to Al. Analysis of global transcriptional responses to Al stress in roots of the NILs alongside their recurrent parents demonstrated that the ART1 from ...
The role of AI interactions with root-cell plasma memhrane (PM) Ca2+ channels in AI toxicity and ... more The role of AI interactions with root-cell plasma memhrane (PM) Ca2+ channels in AI toxicity and resistance was studied. l h e experimental approach involved the imposition of a transmembrane electrical potential (via K+ diffusion) in right-side-out PM vesicles derived from roots of two wheat (Trificum aestivum L.) cultivars (AI-sensitive Scout 66 and AI-resistant Atlas 66). W e previously used this technique to characterize a voltage-dependent Ca" channel in the wheat root PM (J.W. Huang, D.L. Crunes, L.V. Kochian 119941 Proc Natl Acad Sci USA 91: 3473-3477). W e found that AI3+ effectively blocked this P M Cazf channel; however, AI3+ blocked this Ca2+ channel equally well in both the AI-sensitive and-resistant cultivars. I t was found that the differential genotypic sensitivity of this Ca2+ transport system to AI in intact roots versus isolated PM vesicles was due to AI-induced malate exudation localized to the root apex in AI-resistant Atlas but not in AI-sensitive Scout. Because malate can effectively chelate AI3+ in the rhizosphere and exclude it from the root apex, the differential sensitivity of Ca2+ influx to AI in intact roots of AI-resistant versus AI-sensitive wheat cultivars is probahly dueto the maintenance of lower AI3+ activities in the root apical rhizosphere of the resistant cultivar. A1 toxicity is the primary environmental stress limiting crop productivity on acid soils. One of the proposed mechanisms of A1 toxicity involves A1 interaction with ion transport systems functioning at the root-cell PM (Taylor, 1988; Kochian, 1995). The role of A1/Ca2+ transport interactions in the mechanisms of A1 toxicity has recently received considerable attention, because Ca2+ plays a central role in the regulation of many plant cellular processes, including mitosis and cytokinesis, gravitropism, polar growth, and cytoplasmic streaming (Williamson and Ashley, 1982; Hepler and Wayne, 1985). A1 inhibition of Ca2+ influx into plant cells is rapid and reversible, and the A1 blockage of Caz+ influx precedes visible symptoms of A1 toxicity
Proceedings of the National Academy of Sciences of the United States of America, Jan 24, 2017
Members of the aquaporin (AQP) family have been suggested to transport aluminum (Al) in plants; h... more Members of the aquaporin (AQP) family have been suggested to transport aluminum (Al) in plants; however, the Al form transported by AQPs and the roles of AQPs in Al tolerance remain elusive. Here we report that NIP1;2, a plasma membrane-localized member of the Arabidopsis nodulin 26-like intrinsic protein (NIP) subfamily of the AQP family, facilitates Al-malate transport from the root cell wall into the root symplasm, with subsequent Al xylem loading and root-to-shoot translocation, which are critical steps in an internal Al tolerance mechanism in Arabidopsis We found that NIP1;2 transcripts are expressed mainly in the root tips, and that this expression is enhanced by Al but not by other metal stresses. Mutations in NIP1;2 lead to hyperaccumulation of toxic Al(3+) in the root cell wall, inhibition of root-to-shoot Al translocation, and a significant reduction in Al tolerance. NIP1;2 facilitates the transport of Al-malate, but not Al(3+) ions, in both yeast and Arabidopsis We demons...
Radiotracer techniques were employed to characterize 65Zn2+ influx into the root symplasm and tra... more Radiotracer techniques were employed to characterize 65Zn2+ influx into the root symplasm and translocation to the shoot in Thlaspi caerulescens, a Zn hyperaccumulator, and Thlaspi arvense, a nonaccumulator. A protocol was developed that allowed us to quantify unidirectional 65Zn2+ influx across the root-cell plasma membrane (20 min of radioactive uptake followed by 15 min of desorption in a 100 [mu]M ZnCl2 + 5 mM CaCl2 solution). Concentration-dependent Zn2+ influx in both Thlaspi species yielded nonsaturating kinetic curves that could be resolved into linear and saturable components. The linear kinetic component was shown to be cell-wall-bound Zn2+ remaining in the root after desorption, and the saturable component was due to Zn2+ influx across the root-cell plasma membrane. This saturable component followed Michaelis-Menten kinetics, with similar apparent Michaelis constant values for T. caerulescens and T. arvense (8 and 6 [mu]M, respectively). However, the maximum initial veloc...
The relationship between Al-induced depolarization of root-cell transmembrane electrical potentia... more The relationship between Al-induced depolarization of root-cell transmembrane electrical potentials (Em) and Al tolerance in wheat (Triticum aestivum L.) was investigated. Al exposure induced depolarizations of Em in the Al-tolerant wheat cultivars Atlas and ET3, but not in the Al-sensitive wheat cultivars Scout and ES3. The depolarizations of Em occured in root cap cells and as far back as 10 mm from the root tip. The depolarization was specific to Al3+; no depolarization was observed when roots were exposed to the rhizotoxic trivalent cation La3+. The Al-induced depolarization occurred in the presence of anion-channel antagonists that blocked the release of malate, indicating that the depolarization is not due to the electrogenic efflux of malate2-. K+-induced depolarizations in the root cap were of the same magnitude as Al-induced depolarizations, but did not trigger malate release, indicating that Al-induced depolarization of root cap cell membrane potentials is probably linked ...
Many plant biologists work on the identification of genes related to abiotic stress resistance, b... more Many plant biologists work on the identification of genes related to abiotic stress resistance, but the term 'stress resistance gene' is widely used without proper definition. Here it is argued that there is a need to update our understanding of this term and for standardization to facilitate integration of research data.
Uploads
Papers by Leon Kochian