Essential Role of Tissue-Specific Proline Synthesis and Catabolism in Growth and Redox Balance at Low Water Potential

Sharma, Sandeep; Villamor, Joji Grace; Verslues, Paul E.

doi:10.1104/pp.111.183210

Cited by 337 publications

(332 citation statements)

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“…Many plants accumulate proline in response to low water potential (ψ w ) and dehydration caused by drought or freezing. The mechanisms by which proline may promote drought resistance include osmoprotectant functions, as well as newly emerging functions of proline metabolism in NADP/NADPH balance and transfer or storage of energy and reducing potential (1)(2)(3). However, the overall importance of proline in drought adaptation is not as firmly established.…”

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confidence: 99%

Intron-mediated alternative splicing of Arabidopsis P5CS1 and its association with natural variation in proline and climate adaptation

Kesari

Lasky

Villamor

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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Drought-induced proline accumulation is widely observed in plants but its regulation and adaptive value are not as well understood. Proline accumulation of the Arabidopsis accession Shakdara (Sha) was threefold less than that of Landsberg erecta (Ler) and quantitative trait loci mapping identified a reduced function allele of the proline synthesis enzyme Δ 1 -pyrroline-5-carboxylate synthetase1 (P5CS1) as a basis for the lower proline of Sha. Sha P5CS1 had additional TA repeats in intron 2 and a G-to-T transversion in intron 3 that were sufficient to promote alternative splicing and production of a nonfunctional transcript lacking exon 3 (exon 3-skip P5CS1). In Sha, and additional accessions with the same intron polymorphisms, the nonfunctional exon 3-skip P5CS1 splice variant constituted as much as half of the total P5CS1 transcript. In a larger panel of Arabidopsis accessions, low water potential-induced proline accumulation varied by 10-fold and variable production of exon 3-skip P5CS1 among accessions was an important, but not the sole, factor underlying variation in proline accumulation. Population genetic analyses suggest that P5CS1 may have evolved under positive selection, and more extensive correlation of exon 3-skip P5CS1 production than proline abundance with climate conditions of natural accessions also suggest a role of P5CS1 in local adaptation to the environment. These data identify a unique source of alternative splicing in plants, demonstrate a role of exon 3-skip P5CS1 in natural variation of proline metabolism, and suggest an association of P5CS1 and its alternative splicing with environmental adaptation.amino acid metabolism | drought adaptation | stress gene expression | osmoprotectant | compatible solute P roline acts as an osmoprotectant and cryoprotectant in organisms as diverse as bacteria, plants, and insects (1, 2). Many plants accumulate proline in response to low water potential (ψ w ) and dehydration caused by drought or freezing. The mechanisms by which proline may promote drought resistance include osmoprotectant functions, as well as newly emerging functions of proline metabolism in NADP/NADPH balance and transfer or storage of energy and reducing potential (1-3). However, the overall importance of proline in drought adaptation is not as firmly established. In Arabidopsis thaliana, transcriptional up-regulation of Δ 1 -pyrroline-5-carboxylate synthetase1 (P5CS1) is essential for low ψ w -induced proline accumulation, and proline accumulation of p5cs1 mutants is only 15-20% of the wild-type level (4-6). Additional regulation of proline metabolism is likely but not understood. The timing and duration of water limitation, as well as other environmental variables, all influence drought-adaptation strategies used by plants. Thus, we may expect substantial natural variation of these traits within a widely distributed species, such as Arabidopsis (7-10), with many of these differences related to the local conditions to which a particular accession has adapted (11-13). Several studies ha...

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confidence: 99%

Intron-mediated alternative splicing of Arabidopsis P5CS1 and its association with natural variation in proline and climate adaptation

Kesari

Lasky

Villamor

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

126

140

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“…Thus, diverse management has been studied in other species to increase the proline levels (Purvis and Yelenosky, 1982;Correa et al, 2004;Su and Wu, 2004;Gruzka et al, 2007). Differences in the capacity from the varieties in the synthesis of this amino acid (Hanson et al, 1977), their implications for genetic improvement (Nolte and Hanson, 1997) and the genes involved in their transportation (Schwacke et al, 1999;Sharma et al, 2011) have been also researched, showing some interesting elements, mainly by studying the transportation of proline towards the fruits and increased expression of this amino acid through the water defi cit (gimeno et al, 2009). …”

Section: Resultsmentioning

confidence: 99%

“…Lower temperatures would favor an increase of this amino acid in the plant and the difference in temperature possibly generated between each exposure, might be insignificant to induce differences in the proline contents in fruits. Additionally, it needs to be considered that the production of this amino acid does not occur in the fruit, but produced initially in the leaves and then transported to the fruit (Talmadge et al, 1973) via phloem (Sharma et al, 2011). Therefore, if the plant is exposed to lower temperatures in some of the two exposures, it might stimulate the proline synthesis through the entire tree, distributing homogeneously and not only in one sector.…”

Section: Proline Content In Fruits Modified By Exposurementioning

confidence: 99%

“…Tadeo (2000) indicates that this amino acid maintains the membrane permeability favoring microviscosity or optimal flow. Hamilton and Heckathorn (2001) and, Sharma andDietz (2006, cited by Gruzka et al, 2007) remark its antioxidant function, regulating capacity of the potential redox and defence against oxygen reactives, as well as its role on strengthening the membrane integrity (Hanson et al, 1977). It has been also indicated as a protective agent against desiccation and osmotic element in the cell (Purvis, 1981) and as an important way of energy to recover from stress (Sells and Koeppe, 1981;Kavi-Kishort et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

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Peteca rind pitting as influenced by proline content in winter lemon albedo

Fichet

Chamorro²,

Riquelme

2012

Cienc. Inv. Agr.

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T. Fichet, J. Chamorro, and A. Riquelme. 2012. Peteca rind pitting as influenced by proline content in winter lemon albedo. Cien. Inv. Agr. 39(1): 201-209. One of the most important problems in lemon growing is the physiological disorder known as "peteca", which is characterized by causing cell dehydration and death in the albedo tissue with a subsequent necrosis of the surface zone of the fruit. This damage shows characteristics quite similar to those resulting from chilling injury in citrus fruit, where surface damage of fruit and dehydration of albedo cells also occur. Resistance to chilling injury shown by grapefruit would be related to increased proline content in the albedo (Purbis, 1981). In this study, proline content of lemons cv. "Fino" 49 from two groves, one in Curacaví (33°25.778 S -71°02.292 W, 196 m above sea level) and the other in Mallarauco (33°94.984 S -70°58.921 W, 269 m above sea level), was analyzed and determined. The Curacaví grove had a low incidence of peteca, whereas the Mallarauco grove exhibited a high incidence of this disorder. Significant differences in albedo proline content were found between both groves and content of this amino acid was highly associated to the degree of peteca incidence. Proline might be playing a role in the lower incidence of "peteca" in winter lemon fruit.

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“…Root morphological traits are fundamental for multiple functions that are at the basis of plant productivity, which including efficiency of water and inorganic nutrients absorption, root development directly affects the growth and biomass production, and is important factor of the high and stable yield in plants (Sharma et al, 2011). The effect of root architecture on yield and related traits and its role in increasing drought tolerance have been widely reported for all major crops (Tuberosa et al, 2002a, b;de Dorlodot et al, 2007, Christopher et al, 2013.…”

Section: Introductionmentioning

confidence: 99%

Detection of consensus genomic regions associated with root architecture of bread wheat on groups 2 and 3 chromosomes using QTL meta–analysis

Darzi-Ramandi¹,

Shariati²,

Tavakol³

et al. 2017

Aust J Crop Sci

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Root architecture is an important bread wheat phenomenon that highly influences its production and adaptation to environmental stresses, in particular drought stress. Several QTL studies have been conducted to ascertain chromosomal regions associated with root morphology resulting in identification of various loci depending on evaluated population types and experimental conditions. In order to identify the most consistent and reliable QTLs involved in various root morphological traits in bread wheat, a meta-QTL (MQTL) analysis was performed using 106 QTLs derived from 12 different populations under both normal and drought stress conditions. Among them, 125 QTLs related to root traits were successfully projected onto the reference map and further metaanalysis was focused on chromosomes of homeologous groups 2 and 3 with most assigned QTLs. Consequently, a total of seven MQTLs were identified on chromosomes 2A, 2B, 3A and 3B originated from 2 to 17 initial QTLs with a confidence interval (CI) of 5.3-6.6 to 39.5-55.0 cM. Three MQTLs located on 2A, 3A and 3B derived from 7 to 17 QTLs related to different root morphological traits pointed out the most important chromosomal regions. A reduction in the average 95% confidence interval from 20.8 cM to 6.4 cM was observed when comparing the individual QTL to the MQTL. Further analysis on investigation of candidate genes located in these genomic regions resulted in identification of some genes mainly associated with lignin catabolic process, potassium transporters and leucine-rich repeats receptor-like kinases (LRR-RLKs). These results provid fundamental information on most important genomic regions and candidate genes related to root morphology in bread wheat.

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Essential Role of Tissue-Specific Proline Synthesis and Catabolism in Growth and Redox Balance at Low Water Potential

Cited by 337 publications

References 70 publications

Intron-mediated alternative splicing of Arabidopsis P5CS1 and its association with natural variation in proline and climate adaptation

Intron-mediated alternative splicing of Arabidopsis P5CS1 and its association with natural variation in proline and climate adaptation

Peteca rind pitting as influenced by proline content in winter lemon albedo

Detection of consensus genomic regions associated with root architecture of bread wheat on groups 2 and 3 chromosomes using QTL meta–analysis

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