Abstract
The use of iron-efficient rootstocks can be a sustainable way to enhance iron (Fe) fruit content in tomato. A hybrid tomato variety was grafted on a genotyped population of recombinant inbred lines derived from Solanum pimpinellifolium, and compared with self- and non-grafted controls under low iron (5.2 µM) growing conditions. Rootstock effects on total fruit yield, fruit [Fe] and yield Fe content (FeUEc) were the target traits; other minerals were also investigated by quantitative trait loci (QTL) and candidate gene analyses. The rootstock genotype affected fruit concentrations of Fe, Ca, Mg, Mn, Na, P, S, Si and Al. Most rootstocks increased FeUEc. Fruit and leaf [Fe] and FeUEc were genetically complex, involving epistatic interactions. Six and eight QTLs were detected for these traits, respectively, by multiple QTL mapping. Two kinds of relevant genes were found among candidates within QTLs for iron related traits: those coding for secretory proteins specific of the tomato xylem sap under iron deficiency, and others having a role in iron uptake such as TOMLHA1, FRO1, NRAMP2, FER and MYB72. Detected QTLs might reflect differences in the regulatory regions of those relevant genes, more than in their coding sequences.
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References
Asins MJ, Raga V, Roca D, Carbonell EA (2015) Genetic dissection of tomato rootstock effects on scion traits under moderate salinity. Theor Appl Genet 128:667–679
Asins MJ, Albacete A, Martinez-Andujar C, Pérez-Alfocea F, Dodd IC, Carbonell EA, Dieleman JA (2017) Genetic analysis of rootstock-mediated nitrogen (N) uptake and root-to-shoot signalling at contrasting N availabilities in tomato. Plant Sci 263:94–106
Aubry E, Dinant S, Vilaine F, Bellini C, Le Hir R (2019) Lateral transport of organic and inorganic solutes. Plants 8:20. https://doi.org/10.3390/plants8010020
Kevei Z, King RC, Mohareb F, Sergeant MJ, Awan SZ, Thompson AJ (2015) Resequencing at ≥ 40-fold depth of the parental genomes of a Solanum lycopersicum x S. pimpinellifolium recombinant inbred line population and characterization of frame-shift indels that are highly likely to perturb protein function. G3 Genes/Genomes/Genetics 5:971–981
Barberon M, Vermeer JE, De Bellis D, Wang P, Naseer S, Andersen TG, Humbel BM, Nawrath C, Takano J, Salt DE, Geldner N (2016) Adaptation of root function by nutrient-induced plasticity of endodermal differentiation. Cell 164:447–459. https://doi.org/10.1016/j.cell.2015.12.021
Briat J-F, Duc C, Ravet K, Gaymard F (2010) Ferritins and iron storage in plants. Biochem Biophys Acta 1800:806–8014
Capel C, Yuste-Lisbona FJ, López-Casado C, Angost T, Heredia A, Cuarter J, Fernándserz-Muñoz R, Lozano R, Capel J (2017) QTL mapping of fruit mineral contents provides new chances for molecular breeding of tomato nutritional traits. Theor Appl Genet 130:903–913
Castaings L, Caquot A, Loubet S, Curie C (2016) The high-affinity metal transporters NRAMP1 and IRT1 team up to take up iron under sufficient provision. Sci Rep 6:37222. https://doi.org/10.1038/srep37222
Ceballos-Laita L, Gutierrez-Carbonell E, Takahashi D, Abadia A, Uemura M, Abadia J, Lopez-Millan AF (2018) Effects of Fe and Mn deficiencies on the protein profiles of tomato (Solanum lycopersicum) xylem sap as revealed by shotgun analyses. J Proteom 170:117–129. https://doi.org/10.1016/j.jprot.2017.08.018
Clemens S, Weber M (2015) The essential role of coumarin secretion for Fe acquisition from alkaline soil. Plant Signal Behav 11(2):e1114197
Connort JM, Balk J, Rodriguez-Celma J (2017) Iron homeostasis in plants—a brief overview. Metallomics 9:813–823
Davies JN, Hobson LE (1981) The constituents of tomato fruit, the influence of environment, nutrition and genotype. Crit Rev Food Sci Nutr 15:205–280
EFSA (2008) European Food Safety Agency. Scientific opinion of the panel on food additives, flavourings, processing aids and food contact materials (AFC) on a request from the European Commission on safety of aluminium from dietary intake. The EFSA Journal 754:1–34
Erba D, Casiraghi MC, Ribas-Agustí A, Cáceres R, Marfâ O, Castellari M (2013) Nutritional value of tomatoes (Solanum lycopersicum L.) grown in greenhouse by different agronomic techniques. J Food Compos Anal 31:245–251
Estañ MT, Villalta I, Bolarín MC, Carbonell EA, Asins MJ (2009) Identification of fruit yield loci controlling the salt tolerance conferred by solanum rootstocks. Theor Appl Genet 118:305–312
FAOSTAT (2017) FAO statistical dabases FAOSTAT: suit of food security indicators. http://www.fao.org/faostat/en/#data. Accessed 6 Mar 2019
Farrow SC, Facchini PJ (2014) Functional diversity of 2-oxoglutarate/Fe(II)-dependent dioxygenases in plant metabolism. Front Plant Sci 5:624. https://doi.org/10.3389/fpls.2014.00524
Fourcroy P, Sisó-Terraza P, Sudre D, Savirón M, Reyt G, Gaymard F et al (2014) Involvement of the ABCG37 transporter in secretion of scopoletin and derivatives by Arabidopsis roots in response to iron deficiency. New Phytol 201:155–167
Fourcroy P, Tissot N, Gaymard F, Briat JF, Dubos C (2016) Facilitated Fe nutrition by phenolic compounds excreted by the Arabidopsis ABCG37/PDR9 transporter requires the IRT1/FRO2 high-affinity root Fe(2+) transport system. Mol Plant 9:485–488. https://doi.org/10.1016/j.molp.2015.09.010
Gollhaofer J, Timofeev R, Lan P, Schmidt W, Buckhout TJ (2014) Vacuolar-iron-transporter1-like proteins mediate iron homeostasis in Arabidopsis. PloS ONE 9:e110468. https://doi.org/10.1371/journal.pone.0110468
Green LS, Rogers EE (2004) FRD3 controls iron localization in Arabidopsis. Plant Physiol 136:2523–2531. https://doi.org/10.1104/pp.104.045633
Ikeda H, Shibuya T, Nishiyama M, Nakata Y, Kanayama Y (2017) Physiological mechanisms accounting for the lower incidence of blossom-end rot in tomato introgression line IL8-3 fruit. Hortic J 86:327–333
Iqbal N, Trivellini A, Masood A, Ferrante A, Khan NA (2013) Current understanding on ethylene signaling in plants: the influence of nutrient availability. Plant Physiol Biochem 73:128–138
Jaime-Pérez N, Pineda B, García-Sogo B, Atares A, Athman A, Byrt CS, Olias R, Asins MJ, Gilliham M, Moreno V, Belver A (2017) The Na+ transporter encoded by the HKT1;2 gene modulates Na1 +/K+ homeostasis in tomato shoots under salinity. Plant Cell Environ. https://doi.org/10.1111/pce.12883
Kailasam S, Chien W-F, Yeh K-C (2019) Small-molecules selectively modulate iron-deficiency signaling networks in Arabidopsis. Front Plant Sci 10:8. https://doi.org/10.3389/fpls.2019.00008
Kobayashi T, Nishizawa NK (2012) Iron uptake, translocation, and regulation in higher plants. Ann Rev Plant Biolol 63:131–152
Li W, Lan P (2017) The understanding of the plant iron deficiency responses in Strategy I plants and the role of ethylene in this process by omic approaches. Front Plant Sci 8:40. https://doi.org/10.3389/fpls.2017.00040
Lin HX, Rubio L, Smythe AB, Falk BW (2004) Molecular population genetics of Cucumber mosaic virus in California: Evidence for founder effects and reassortment. J Virol 78:6666–6675
Lin XY, Ye YQ, Fan SK, Jin CW, Zheng SJ (2016) Increased sucrose accumulation regulates iron-deficiency responses by promoting auxin signaling in Arabidopsis plants. Plant Physiol 170:907–920. https://doi.org/10.1104/pp15.01598
Liu XX, He XL, Jin CW (2016) Roles of chemical signals in regulation of the adaptive responses to iron deficiency. Plant Signal Behav 11:e1179418. https://doi.org/10.1080/15592324.2016.1179418
Lucena C, Waters BM, Romera FJ, Garcia MJ, Morales M, Alcántara E, Pérez-Vicente R (2006) Ethylene could influence ferric reductase, iron transporter, and H+-ATPase gene expression by affecting FER (or FER-like) gene activity. J Exp Bot 57:4145–4154
McLean E, Cogswell M, Egli I, Woidyla D, De Benoist B (2009) Worlwide prevalence of anaemia. WHO vitamin and mineral nutrition information system, 1993–2005. Public Health Nutr 12:444–454. https://doi.org/10.1017/S1368980008002401
Meenakshi JV, Johnson NL, Manyong VM, Degroote H, Javelosa J, Yaggen DR et al (2010) Hoe cost-effective is biofortification in combating micronutrient malnutrition? An ex ante assessment. World Dev 38:64–75
Mengel K (1994) Iron availability in plant-tissues-iron chlorosis on calcareous soils. Plant Soil 165:275–283
Mi H, Muruganujan A, Casagrande JT, Thomas PD (2013) Large-scale gene function analysis with the PANTHER classification system. Nat Protoc 8:1551–1566
Mi H, Huang X, Muruganujan A, Tang H, Mills C, Kang D, Thomas PD (2016) PANTHER version 11: expanded annotation data from gene ontology and reactome pathways, and data analysis tool enhancements. Nucleic Acids Res. https://doi.org/10.1093/nar/gkw1138
Michalak P (2008) Coexpression, coregulation, and cofunctionality of neighboring genes in eukaryotic genomes. Genomics 9:243–248
Miller DD, Welch RM (2013) Foods system strategies for preventing micronutrient malnutrition. Food Policy 42:115–128. https://doi.org/10.1016/j.foodpol.2013.06.008
Monforte AJ, Asins MJ, Carbonell EA (1997) Salt tolerance in Lycopersicon species. 5. Does genetic variability at quantitative trait loci affect their analysis? Theor Appl Genet 95:284–293
Mora-Macías J, Jo Ojeda-Rivers, Gutierrez-Alanis D, Yong-Villalobos L, Oropeza-Aburto A, Raya-González J et al (2017) Malate-dependent Fe accumulation is a critical checkpoint in the root development response to low phosphate. Proc Natl Acad Sci USA 114:E3563–E3572
O’Rourke JA, Nelson RT, Grant D, Schmutz J, Grimwood J, Cannon S, Vance CP, Shoemaker RC (2009) Integrating microarray analysis and the soybean genome to understand the soybeans iron deficiency response. BMC Genom 10:376. https://doi.org/10.1186/1471-2164-10-376
Peuke AD (2010) Correlations in concentrations, xylem and phloem flows, and partitioning of elements and ions in intact plants. A summary and statistical re-evaluation of modelling experiments in Ricinus communis. J Exp Bot 61:635–655
Plouznikoff K, Asins MJ, Dupré de Boulois H, Carbonell EA, Declerck S (2019) Genetic analysis of tomato root colonization by arbuscular mycorrhizal fungi. Ann Bot. https://doi.org/10.1093/aob/mcy240
Price AH (2006) Believe it or not, QTLs are accurate! Trends Plant Sci 11:213–216
Rellan-Alvarez R, Giner-Martinez-Sierra J, Orduna J, Orera I, Rodriguez-Castrillon JA, Garcia-Alonso JI, Abadia J, Alvarez-Fernandez A (2010) Identification of a tri-iron (III), tri-citrate complex in the xylem sap of iron-deficient tomato resupplied with iron: new insights into plant iron long-distance transport. Plant Cell Physiol 51:91–102. https://doi.org/10.1093/pcp/pcp170
Rellan-Alvarez R, El-Jendoubi H, Wohlgemuth G, Abadia A, Fiehn O, Abadia J, Alvarez-Fernandez A (2011) Metabolite profile changes in xylem sap and leaf extracts of strategy I plants in response to iron deficiency and resupply. Front Plant Sci 2:66. https://doi.org/10.3389/fpls.2011.00066
Romera FJ, García MJ, Lucena C, Martínez-Medina A, Aparicio MA, Ramos J, Alcántara E, Angulo M, Pérez-Vicente R (2019) Induced systemic resistance (ISR) and Fe deficiency responses in dicot plants. Front Plant Sci 10:287
Santi S, Schmidt W (2009) Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots. New Phytol 183:1072–1084
Strobbe S, De Lepeleire J, Van Der Straeten D (2018) From in planta function to vitamin-rich food crops: the ACE of biofortification. Front Plant Sci 9:1862. https://doi.org/10.3389/fpls.2018.01862
Tsai H, Schmidt W (2017) Mobilization of iron by plant-borne coumarins. Trends Plant Sci 22:538–548
Uozumi A, Ikeda H, Hiraga M (2012) Tolerance to salt stress and blossom-end rot in an introgression line, IL8-3, of tomato. Sci Hortic 138:1–6
Van Ooijen JW (2009) MapQTL 6. Software for the mapping of quantitative trait loci in experimental populations of diploid species. Kyazma BV, Wageningen, Netherlands
Villalta I, Bernet GP, Carbonell EA, Asins MJ (2007) Comparative QTL analysis of salinity tolerance in terms of fruit yield using two Solanum populations of F7 lines. Theor Appl Genet 114:1001–1017
Wang H, Inukaia Y, Yamauchia A (2006) Root development and nutrient uptake. Crit Rev Plant Sci 25:279–301
Waters BM, Amundsen K, Graef G (2018) Gene expression profiling on iron deficiency chlorosis sensitive and tolerant soybean indicates key roles for phenylpropanoids under alkalinity stress. Front Plant Sci 9:10. https://doi.org/10.3389/fpls.2018.00010
Zamboni A, Zanin L, Tomasi N, Pezzotti M, Pinton R, Varanin Z, Cesco S (2012) Genome-wide microarray analysis of tomato roots showed defined responses to iron deficiency. BMC Genom 13:101. https://doi.org/10.1186/1471-2164-13-101
Zhu XF, Wang B, Song WF, Zheng SJ, Shen RF (2016) Putrescine alleviates iron deficiency via NO-dependent reutilization of root cell wall Fe in Arabidopsis. Plant Physiol 170:558–567
Acknowledgements
We thank Mrs. Miryam Rojas at Servicio de Instrumentación Científica de la Estación Experimental del Zaidín (CSIC) for mineral analysis, and Dr. Luis Galipienso (IVIA) for viral tests. This work was supported by grants from the Spanish Government (MJA) (AGL2014-56675-R, AGL2017-82452-C2-2-R), and Fondo Social Europeo de la Comunitat Valenciana (DT) (01/15-FSE-02).
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Supplementary Fig.
1-Course of the experiment; (A), general view of grafted tomato plants grown under commercial conditions but limiting Fe nutrition (March 2017); (B), fruit yield (May 2017); (C), a hand is holding a truss with bronze, deformed tomatoes. (PDF 353 kb)
Supplementary Fig.
2-Relative (A) and absolute (B) mean concentrations of elements at the fruits (left) and leaves (right) of the commercial tomato variety grafted on the recombinant inbred lines. Y axes in B correspond to element concentration in ppm. (PDF 91 kb)
Supplementary Fig.
3-Graphic representation of principal component analysis of variability found among grafted RILs under commercial, iron limiting conditions for vegetative, mineral, and fruit yield and quality traits. Three groups of elements are noted (encircled). (PDF 129 kb)
Supplementary Table
4-Pearson coefficients between significantly correlated traits (p ≤ 0.05). (XLSX 18 kb)
Supplementary Table
5-Summary list of candidate genes for major QTLs (See QTLs with SNP in bold and excluding those related to Fe traits at Table 2), some of them are segregating for frameshift Indels (Kevei et al. 2015) in parental genomes, E9 or L5, (Mut.). The Locus reference, its relative root expression (Exp.) in Heinz cultivar (Max: maximum, H: high, M: medium, VL: very low, L: low and N: no data), and the number of genes counted from the QTL peak (Ord.) are also shown. (XLSX 12 kb)
Supplementary Fig.
6-LOD profiles of QTLs for Fe_L, Fe_F and FeUEc. QTL peaks detected for two traits at the same region are encircled. Genetic positions along the 12 chromosomes are shown under the X axis. (PDF 130 kb)
Supplementary Table
7-Overrepresented Biological processes within QTLs detected for iron related traits by means of the PANTHER Classification System (http://www.pantherdb.org/) using the Fisher´s Exact with FDR multiple test correction. The suffix _All denotes all downloaded genes were considered, while _Seg corresponds to those genes segregating in the RIL population for frameshift mutations only. (XLSX 13 kb)
Supplementary Table
8-List of genes within %Cit_12, the QTL detected for citric acid fruit content in chromosome 12, some segregating for frameshift Indels (Kevei et al. 2015) in parental genomes, E9 or L5, (Mut.). The Locus reference, its relative root expression (Exp.) in Heinz cultivar (Max: maximum, H: high, M: medium, VL: very low, L: low and N: no data), and the number of genes counted from the QTL peak (Ord.) are also shown. (XLSX 23 kb)
Supplementary Table
9-List of genes within QTLs detected for frequency of fruits with blossom end rot (pFNber), some segregating for frameshift Indels (Kevei et al. 2015) in parental genomes, E9 or L5, (Mut.). The Locus reference, its relative root expression (Exp.) in Heinz cultivar (Max: maximum, H: high, M: medium, VL: very low, L: low and N: no data), and the number of genes counted from the QTL peak (Ord.) are also shown. (XLSX 40 kb)
Supplementary Fig.
10-Overrepresented molecular functions within blossom end rot QTLs by means of the PANTHER Classification System (http://www.pantherdb.org/) using the Fisher´s Exact with FDR multiple test correction. (PDF 171 kb)
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Asins, M.J., Raga, M.V., Torrent, D. et al. QTL and candidate gene analyses of rootstock-mediated tomato fruit yield and quality traits under low iron stress. Euphytica 216, 63 (2020). https://doi.org/10.1007/s10681-020-02599-6
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DOI: https://doi.org/10.1007/s10681-020-02599-6