Advances in Iron Deficiency-induced Coumarin Biosynthesis and Their Functions in Iron Absorption in Plants
Received date: 2024-07-17
Accepted date: 2024-12-14
Online published: 2024-12-27
Coumarins are a class of phenolic compounds with benzopyrones as the parent ring structure, categorized into simple and complex coumarins, and widely distributed in higher plants. In recent years, studies have shown that root-secreted coumarins can promote iron absorption in plants. Here, the recent progress in the discovery and identification of genes related to the biosynthesis and regulation of plant iron deficiency-induced coumarins is reviewed, and the molecular mechanisms of the biosynthesis, storage, secretion, and regulation of iron deficiency-induced coumarins are further elaborated. The mechanism by which coumarins could promote plant iron uptake has also been discussed. Finally, this paper provides a preliminary outlook on the future research directions to gain knowledge of these mechanisms, which could offer novel opportunities to generate iron deficiency-tolerant crops and iron-biofortified crops.
Key words： iron deficiency; coumarin; biosynthesis; regulation; iron uptake
Zhou Jing , Gao Fei . Advances in Iron Deficiency-induced Coumarin Biosynthesis and Their Functions in Iron Absorption in Plants[J]. Chinese Bulletin of Botany, 2025 , 60(3) : 460 -471 . DOI: 10.11983/CBB24106
| [1] | Ahn YO, Shimizu BI, Sakata K, Gantulga D, Zhou Z, Bevan DR, Esen A (2010). Scopolin-hydrolyzing β-glucosidases in roots of Arabidopsis. Plant Cell Physiol 51, 132-143. |
| [2] | Bauer P, Ling HQ, Guerinot ML (2007). FIT, the FER-like iron deficiency induced transcription factor in Arabidopsis. Plant Physiol Biochem 45, 260-261. |
| [3] | Briat JF, Dubos C, Gaymard F (2015). Iron nutrition, biomass production, and plant product quality. Trends Plant Sci 20, 33-40. |
| [4] | Brown JC, Ambler JE (1973). “Reductants” released by roots of Fe-deficient soybeans. Agron J 65, 311-314. |
| [5] | Brumbarova T, Bauer P, Ivanov R (2015). Molecular mechanisms governing Arabidopsis iron uptake. Trends Plant Sci 20, 124-133. |
| [6] | Carvalhais LC, Dennis PG, Fedoseyenko D, Hajirezaei MR, Borriss R, von Wirén N (2011). Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency. J Plant Nutr Soil Sci 174, 3-11. |
| [7] | Chezem WR, Memon A, Li FS, Weng JK, Clay NK (2017). SG2-type R2R3-MYB transcription factor MYB15 controls defense-induced lignification and basal immunity in Arabidop-sis. Plant Cell 29, 1907-1926. |
| [8] | Chutia R, Abel S, Ziegler J (2019). Iron and phosphate deficiency regulators concertedly control coumarin profiles in Arabidopsis thaliana roots during iron, phosphate, and combined deficiencies. Front Plant Sci 10, 113. |
| [9] | Colangelo EP, Guerinot ML (2004). The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response. Plant Cell 16, 3400-3412. |
| [10] | de Brito Francisco R, Martinoia E (2018). The vacuolar transportome of plant specialized metabolites. Plant Cell Physiol 59, 1326-1336. |
| [11] | DeLoose M, Cho H, Bouain N, Choi I, Prom-U-Thai C, Shahzad Z, Zheng LQ, Rouached H (2024). PDR9 allelic variation and MYB63 modulate nutrient-dependent coumarin homeostasis in Arabidopsis. Plant J 117, 1716-1727. |
| [12] | Dong NQ, Lin HX (2021). Contribution of phenylpropanoid metabolism to plant development and plant-environment interactions. J Integr Plant Biol 63, 180-209. |
| [13] | Ducos E, Fraysse ?S, Boutry M (2005). NtPDR3, an iron-deficiency inducible ABC transporter in Nicotiana taba-cum. FEBS Lett 579, 6791-6795. |
| [14] | Fourcroy P, Sisó-Terraza P, Sudre D, Savirón M, Reyt G, Gaymard F, Abadía A, Abadia J, álvarez-Fernández A, Briat JF (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. |
| [15] | 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 Fe2+ transport system. Mol Plant 9, 485-488. |
| [16] | Gao F, Dubos C (2021). Transcriptional integration of plant responses to iron availability. J Exp Bot 72, 2056-2070. |
| [17] | Gao F, Robe K, Bettembourg M, Navarro N, Rofidal V, Santoni V, Gaymard F, Vignols F, Roschzttardtz H, Izquierdo E, Dubos C (2020a). The transcription factor bHLH121 interacts with bHLH105 (ILR3) and its closest homologs to regulate iron homeostasis in Arabidopsis. Plant Cell 32, 508-524. |
| [18] | Gao F, Robe K, Dubos C (2020b). Further insights into the role of bHLH121 in the regulation of iron homeostasis in Arabidopsis thaliana. Plant Signal Behav 15, 1795582. |
| [19] | Gao F, Robe K, Gaymard F, Izquierdo E, Dubos C (2019). The transcriptional control of iron homeostasis in plants: a tale of bHLH transcription factors? Front Plant Sci 10, 6. |
| [20] | Guerinot ML, Yi Y (1994). Iron: nutritious, noxious, and not readily available. Plant Physiol 104, 815-820. |
| [21] | H?nsch R, Mendel RR (2009). Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). Curr Opin Plant Biol 12, 259-266. |
| [22] | Hether NH, Olsen RA, Jackson LL (1984). Chemical identification of iron reductants exuded by plant roots. J Plant Nutr 7, 667-676. |
| [23] | Jin CW, You GY, He YF, Tang CX, Wu P, Zheng SJ (2007). Iron deficiency-induced secretion of phenolics facilitates the reutilization of root apoplastic iron in red clover. Plant Physiol 144, 278-285. |
| [24] | Kai K, Mizutani M, Kawamura N, Yamamoto R, Tamai M, Yamaguchi H, Sakata K, Shimizu BI (2008). Scopoletin is biosynthesized via ortho-hydroxylation of feruloyl CoA by a 2-oxoglutarate-dependent dioxygenase in Arabidopsis thaliana. Plant J 55, 989-999. |
| [25] | Knoblauch M, Vendrell M, De Leau E, Paterlini A, Knox K, Ross-Elliot T, Reinders A, Brockman SA, Ward J, Oparka K (2015). Multispectral phloem-mobile probes: properties and applications. Plant Physiol 167, 1211-1220. |
| [26] | Kobayashi T, Nishizawa NK (2012). Iron uptake, translocation, and regulation in higher plants. Annu Rev Plant Biol 63, 131-152. |
| [27] | Lan P, Li WF, Wen TN, Shiau JY, Wu YC, Lin W, Schmidt W (2011). iTRAQ protein profile analysis of Arabidopsis roots reveals new aspects critical for iron homeostasis. Plant Physiol 155, 821-834. |
| [28] | Lefèvre F, Fourmeau J, Pottier M, Baijot A, Cornet T, Abadía J, álvarez-Fernández A, Boutry M (2018). The Nicotiana tabacum ABC transporter NtPDR3 secretes O- methylated coumarins in response to iron deficiency. J Exp Bot 69, 4419-4431. |
| [29] | Leiková A, Giehl RFH, Hartmann A, Fargaiová A, von Wirén N (2017). Heavy metals induce iron deficiency responses at different hierarchic and regulatory levels. Plant Physiol 174, 1648-1668. |
| [30] | Li LM, Wu LH, Ma GR (2010). The progress on iron-absorbing mechanism and related gene in plant. Chin J Soil Sci 41, 994-999. (in Chinese) |
| 李利敏, 吴良欢, 马国瑞 (2010). 植物吸收铁机理及其相关基因研究进展. 土壤通报 41, 994-999. | |
| [31] | Murgia I, Tarantino D, Soave C, Morandini P (2011). Arabidopsis CYP82C4 expression is dependent on Fe availability and circadian rhythm, and correlates with genes involved in the early Fe deficiency response. J Plant Physiol 168, 894-902. |
| [32] | Paffrath V, Tandron Moya YA, Weber G, von Wirén N, Giehl RFH (2024). A major role of coumarin-dependent ferric iron reduction in strategy I-type iron acquisition in Arabidopsis. Plant Cell 36, 642-664. |
| [33] | Pan IC, Tsai HH, Cheng YT, Wen TN, Buckhout TJ, Schmidt W (2015). Post-transcriptional coordination of the Arabidopsis iron deficiency response is partially dependent on the E3 ligases RING DOMAIN LIGASE1 (RGLG1) and RING DOMAIN LIGASE2 (RGLG2). Mol Cell Proteomics 14, 2733-2752. |
| [34] | Rajniak J, Giehl RFH, Chang E, Murgia I, von Wirén N, Sattely ES (2018). Biosynthesis of redox-active metabolites in response to iron deficiency in plants. Nat Chem Biol 14, 442-450. |
| [35] | Riaz N, Guerinot ML (2021). All together now: regulation of the iron deficiency response. J Exp Bot 72, 2045-2055. |
| [36] | Robe K, Conejero G, Gao F, Lefebvre-Legendre L, Sylvestre-Gonon E, Rofidal V, Hem S, Rouhier N, Barberon M, Hecker A, Gaymard F, Izquierdo E, Dubos C (2021a). Coumarin accumulation and trafficking in Arabidopsis thaliana: a complex and dynamic process. New Phytol 229, 2062-2079. |
| [37] | Robe K, Izquierdo E, Vignols F, Rouached H, Dubos C (2021b). The coumarins: secondary metabolites playing a primary role in plant nutrition and health. Trends Plant Sci 26, 248-259. |
| [38] | Rodríguez-Celma J, Lin WD, Fu GM, Abadía J, Lopez-Millan AF, Schmidt W (2013). Mutually exclusive alterations in secondary metabolism are critical for the uptake of insoluble iron compounds by Arabidopsis and Medicago truncatula. Plant Physiol 162, 1473-1485. |
| [39] | Rodríguez-Celma J, Tsai YH, Wen TN, Wu YC, Curie C, Schmidt W (2016). Systems-wide analysis of manganese deficiency-induced changes in gene activity of Arabidopsis roots. Sci Rep 6, 35846. |
| [40] | Rodríguez-Celma J, Vázquez-Reina S, Orduna J, Abadía A, Abadía J, álvarez-Fernández A, López-Millán AF (2011). Characterization of flavins in roots of Fe-deficient strategy I plants, with a focus on Medicago truncatula. Plant Cell Physiol 52, 2173-2189. |
| [41] | R?mheld V, Marschner H (1981). Iron deficiency stress induced morphological and physiological changes in root tips of sunflower. Physiol Plant 53, 354-360. |
| [42] | Ro?mheld V, Marschner H (1983). Mechanism of iron uptake by peanut plants: I. FeIII reduction, chelate splitting, and release of phenolics. Plant Physiol 71, 949-954. |
| [43] | Ro?mheld V, Marschner H (1986). Evidence for a specific uptake system for iron phytosiderophores in roots of gras- ses. Plant Physiol 80, 175-180. |
| [44] | Schmid NB, Giehl RFH, D?ll S, Mock HP, Strehmel N, Scheel D, Kong XL, Hider RC, von Wirén N (2014). Feruloyl-CoA 6′-hydroxylase1-dependent coumarins mediate iron acquisition from alkaline substrates in Arabidopsis. Plant Physiol 164, 160-172. |
| [45] | Schmidt W (1999). Mechanisms and regulation of reduction-based iron uptake in plants. New Phytol 141, 1-26. |
| [46] | Schmidt W (2003). Iron solutions: acquisition strategies and signaling pathways in plants. Trends Plant Sci 8, 188-193. |
| [47] | Schwarz B, Bauer P (2020). FIT, a regulatory hub for iron deficiency and stress signaling in roots, and FIT-dependent and independent gene signatures. J Exp Bot 71, 1694-1705. |
| [48] | Shen HY, Xiong HC, Guo XT, Zuo YM (2011). Progress of molecular and physiological mechanism of iron uptake and translocation in plants. Plant Nutr Fert Sci 17, 1522-1530. (in Chinese) |
| 申红芸, 熊宏春, 郭笑彤, 左元梅 (2011). 植物吸收和转运铁的分子生理机制研究进展. 植物营养与肥料学报 17, 1522-1530. | |
| [49] | Siwinska J, Siatkowska K, Olry A, Grosjean J, Hehn A, Bourgaud F, Meharg AA, Carey M, Lojkowska E, Ihnatowicz A (2018). Scopoletin 8-hydroxylase: a novel enzyme involved in coumarin biosynthesis and iron-deficiency responses in Arabidopsis. J Exp Bot 69, 1735-1748. |
| [50] | Stringlis IA, Yu KE, Feussner K, de Jonge R, Van Bentum S, Van Verk MC, Berendsen RL, Bakker PA, Feussner I, Pieterse CM (2018). MYB72-dependent coumarin exudation shapes root microbiome assembly to promote plant health. Proc Natl Acad Sci USA 115, E5213- E5222. |
| [51] | Takemoto T, Nomoto K, Fushiya S, Ouchi R, Kusano G, Hikino H, Takagi SI, Matsuura Y, Kakudo M (1978). Structure of mugineic acid, a new amino acid possessing an iron-chelating activity from roots washings of water-cultured Hordeum vulgare L. Proc Jpn Acad Ser B 54, 469-473. |
| [52] | Tsai HH, Rodríguez-Celma J, Lan P, Wu YC, Vélez- Bermúdez IC, Schmidt W (2018). Scopoletin 8-hydroxylase-mediated fraxetin production is crucial for iron mobi- lization. Plant Physiol 177, 194-207. |
| [53] | Tsai HH, Schmidt W (2017). Mobilization of iron by plant- borne coumarins. Trends Plant Sci 22, 538-548. |
| [54] | Vanholme R, Sundin L, Seetso KC, Kim H, Liu XY, Li J, De Meester B, Hoengenaert L, Goeminne G, Morreel K, Haustraete J, Tsai HH, Schmidt W, Vanholme B, Ralph J, Boerjan W (2019). COSY catalyses trans-cis isomerization and lactonization in the biosynthesis of coumarins. Nat Plants 5, 1066-1075. |
| [55] | Vogt T (2010). Phenylpropanoid biosynthesis. Mol Plant 3, 2-20. |
| [56] | Waters BM, Amundsen K, Graef G (2018). Gene expression profiling of iron deficiency chlorosis sensitive and tolerant soybean indicates key roles for phenylpropanoids under alkalinity stress. Front Plant Sci 9, 10. |
| [57] | Welkie GW (2000). Taxonomic distribution of dicotyledonous species capable of root excretion of riboflavin under iron deficiency. J Plant Nutr 23, 1819-1831. |
| [58] | Werner C, Matile P (1985). Accumulation of coumarylglucosides in vacuoles of barley mesophyll protoplasts. J Plant Physiol 118, 237-249. |
| [59] | World Health Organization (2003). Diet, Nutrition and the Prevention of Chronic Diseases. Geneva: WHO. pp. 1-149. |
| [60] | Wu HL, Wang N, Ling HQ (2007). Uptake, translocation and regulation of iron in plants. Chin Bull Bot 24, 779-788. (in Chinese) |
| 吴慧兰, 王宁, 凌宏清 (2007). 植物铁吸收、转运和调控的分子机制研究进展. 植物学通报 24, 779-788. | |
| [61] | Xu WJ, Dubos C, Lepiniec L (2015). Transcriptional control of flavonoid biosynthesis by MYB-bHLH-WDR complexes. Trends Plant Sci 20, 176-185. |
| [62] | Yang TJW, Lin WD, Schmidt W (2010). Transcriptional profiling of the Arabidopsis iron deficiency response reveals conserved transition metal homeostasis networks. Plant Physiol 152, 2130-2141. |
| [63] | Zamioudis C, Hanson J, Pieterse CMJ (2014). β-glucosidase BGLU42 is a MYB72-dependent key regulator of rhizobacteria-induced systemic resistance and modulates iron deficiency responses in Arabidopsis roots. New Phytol 204, 368-379. |
| [64] | Zhang XB, Gou MY, Guo CR, Yang H, Liu CJ (2015). Down-regulation of Kelch domain-containing F-box protein in Arabidopsis enhances the production of (poly) phe- nols and tolerance to ultraviolet radiation. Plant Physiol 167, 337-350. |
| [65] | Zhang XB, Gou MY, Liu CJ (2013). Arabidopsis Kelch repeat F-box proteins regulate phenylpropanoid biosynthesis via controlling the turnover of phenylalanine ammonia-lyase. Plant Cell 25, 4994-5010. |
| [66] | Zhao AN, Luo GM, Luo YJ, Song DD, Xia HD, Ren HM, Zhang P (2021). Mechanism of bHLH transcription factors in the regulatory network of plant iron deficiency. J Agric Biotechnol 29, 2427-2435. (in Chinese) |
| 赵安娜, 罗光明, 罗扬婧, 宋丹丹, 夏鸿东, 任洪曼, 张攀 (2021). bHLH转录因子在植物缺铁调控网络中的作用机制. 农业生物技术学报 29, 2427-2435. | |
| [67] | Ziegler J, Schmidt S, Chutia R, Müller J, B?ttcher C, Strehmel N, Scheel D, Abel S (2016). Non-targeted profiling of semi-polar metabolites in Arabidopsis root exudates uncovers a role for coumarin secretion and lignification during the local response to phosphate limitation. J Exp Bot 67, 1421-1432. |
| [68] | Ziegler J, Schmidt S, Strehmel N, Scheel D, Abel S (2017). Arabidopsis transporter ABCG37/PDR9 contributes primarily highly oxygenated coumarins to root exudation. Sci Rep 7, 3704. |
/
| 〈 |
|
〉 |
Home