Salicylic Acid Mediates the Reduced Growth of Lignin Down-regulated Plants

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2011 Nov 30

PMID 22123972

Citations 74

Authors

Lina Gallego-Giraldo

Luis Escamilla-Trevino

Lisa A Jackson

Richard A Dixon

Affiliations

Soon will be listed here.

Abstract

Down-regulation of the enzyme hydroxycinnamoyl CoA: shikimate hydroxycinnamoyl transferase (HCT) in thale cress (Arabidopsis thaliana) and alfalfa (Medicago sativa) leads to strongly reduced lignin levels, reduced recalcitrance of cell walls to sugar release, but severe stunting of the plants. Levels of the stress hormone salicylic acid (SA) are inversely proportional to lignin levels and growth in a series of transgenic alfalfa plants in which lignin biosynthesis has been perturbed at different biosynthetic steps. Reduction of SA levels by genetically blocking its formation or causing its removal restores growth in HCT-down-regulated Arabidopsis, although the plants maintain reduced lignin levels. SA-mediated growth inhibition may occur via interference with gibberellic acid signaling or responsiveness. Our data place SA as a central component in growth signaling pathways that either sense flux into the monolignol pathway or respond to secondary cell-wall integrity, and indicate that it is possible to engineer plants with highly reduced cell-wall recalcitrance without negatively impacting growth.

Citing Articles

Integrated physiological and transcriptomic analyses reveal that cell wall biosynthesis and expansion play an important role in the regulation of plant height in alfalfa.

Jing F, Shi S, Kang W, Wu B, Lu B, Guan J BMC Plant Biol. 2025; 25(1):267.

PMID: 40021950 PMC: 11869670. DOI: 10.1186/s12870-025-06172-y.

Understanding metabolic diversification in plants: branchpoints in the evolution of specialized metabolism.

Ji W, Osbourn A, Liu Z Philos Trans R Soc Lond B Biol Sci. 2024; 379(1914):20230359.

PMID: 39343032 PMC: 11439499. DOI: 10.1098/rstb.2023.0359.

The miR7125-MdARF1 module enhances the resistance of apple to Colletotrichum gloeosporioides by promoting lignin synthesis in response to salicylic acid signalling.

Liu X, Dai H, Zhang F, Wang J, Shi J, Chen J Plant Biotechnol J. 2024; 22(10):2741-2755.

PMID: 38852059 PMC: 11536455. DOI: 10.1111/pbi.14401.

The Laccase Family Gene Participates in Resistance to Infection in Tea Plants.

Li D, Zhang H, Zhou Q, Tao Y, Wang S, Wang P Plants (Basel). 2024; 13(6).

PMID: 38592904 PMC: 10975366. DOI: 10.3390/plants13060884.

How plants manage pathogen infection.

Jian Y, Gong D, Wang Z, Liu L, He J, Han X EMBO Rep. 2024; 25(1):31-44.

PMID: 38177909 PMC: 10897293. DOI: 10.1038/s44319-023-00023-3.

References

Hoffmann L, Besseau S, Geoffroy P, Ritzenthaler C, Meyer D, Lapierre C . Silencing of hydroxycinnamoyl-coenzyme A shikimate/quinate hydroxycinnamoyltransferase affects phenylpropanoid biosynthesis. Plant Cell. 2004; 16(6):1446-65. PMC: 490038. DOI: 10.1105/tpc.020297. View

Chen Z, Zheng Z, Huang J, Lai Z, Fan B . Biosynthesis of salicylic acid in plants. Plant Signal Behav. 2009; 4(6):493-6. PMC: 2688294. DOI: 10.4161/psb.4.6.8392. View

Li X, Bonawitz N, Weng J, Chapple C . The growth reduction associated with repressed lignin biosynthesis in Arabidopsis thaliana is independent of flavonoids. Plant Cell. 2010; 22(5):1620-32. PMC: 2899864. DOI: 10.1105/tpc.110.074161. View

Zhou R, Jackson L, Shadle G, Nakashima J, Temple S, Chen F . Distinct cinnamoyl CoA reductases involved in parallel routes to lignin in Medicago truncatula. Proc Natl Acad Sci U S A. 2010; 107(41):17803-8. PMC: 2955080. DOI: 10.1073/pnas.1012900107. View

Bari R, Jones J . Role of plant hormones in plant defence responses. Plant Mol Biol. 2008; 69(4):473-88. DOI: 10.1007/s11103-008-9435-0. View

Cao H, Glazebrook J, Clarke J, Volko S, Dong X . The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell. 1997; 88(1):57-63. DOI: 10.1016/s0092-8674(00)81858-9. View

Nawrath C, Metraux J . Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell. 1999; 11(8):1393-404. PMC: 144293. DOI: 10.1105/tpc.11.8.1393. View

Achard P, Cheng H, De Grauwe L, Decat J, Schoutteten H, Moritz T . Integration of plant responses to environmentally activated phytohormonal signals. Science. 2006; 311(5757):91-4. DOI: 10.1126/science.1118642. View

Besseau S, Hoffmann L, Geoffroy P, Lapierre C, Pollet B, Legrand M . Flavonoid accumulation in Arabidopsis repressed in lignin synthesis affects auxin transport and plant growth. Plant Cell. 2007; 19(1):148-62. PMC: 1820963. DOI: 10.1105/tpc.106.044495. View

10.

Gaffney T, Friedrich L, Vernooij B, Negrotto D, Nye G, Uknes S . Requirement of salicylic Acid for the induction of systemic acquired resistance. Science. 1993; 261(5122):754-6. DOI: 10.1126/science.261.5122.754. View

11.

Rivas-San Vicente M, Plasencia J . Salicylic acid beyond defence: its role in plant growth and development. J Exp Bot. 2011; 62(10):3321-38. DOI: 10.1093/jxb/err031. View

12.

Shadle G, Chen F, Srinivasa Reddy M, Jackson L, Nakashima J, Dixon R . Down-regulation of hydroxycinnamoyl CoA: shikimate hydroxycinnamoyl transferase in transgenic alfalfa affects lignification, development and forage quality. Phytochemistry. 2007; 68(11):1521-9. DOI: 10.1016/j.phytochem.2007.03.022. View

13.

Ryals J, Neuenschwander U, Willits M, Molina A, Steiner H, HUNT M . Systemic Acquired Resistance. Plant Cell. 1996; 8(10):1809-1819. PMC: 161316. DOI: 10.1105/tpc.8.10.1809. View

14.

Huang W, Wang H, Zheng H, Huang L, Singer A, Thompson I . Chromosomally located gene fusions constructed in Acinetobacter sp. ADP1 for the detection of salicylate. Environ Microbiol. 2005; 7(9):1339-48. DOI: 10.1111/j.1462-5822.2005.00821.x. View

15.

Franke R, Humphreys J, Hemm M, Denault J, Ruegger M, Cusumano J . The Arabidopsis REF8 gene encodes the 3-hydroxylase of phenylpropanoid metabolism. Plant J. 2002; 30(1):33-45. DOI: 10.1046/j.1365-313x.2002.01266.x. View

16.

Dewdney J, Reuber T, Wildermuth M, Devoto A, Cui J, Stutius L . Three unique mutants of Arabidopsis identify eds loci required for limiting growth of a biotrophic fungal pathogen. Plant J. 2000; 24(2):205-18. DOI: 10.1046/j.1365-313x.2000.00870.x. View

17.

Shah J, Kachroo P, Nandi A, Klessig D . A recessive mutation in the Arabidopsis SSI2 gene confers SA- and NPR1-independent expression of PR genes and resistance against bacterial and oomycete pathogens. Plant J. 2001; 25(5):563-74. DOI: 10.1046/j.1365-313x.2001.00992.x. View

18.

Lee Y, Chen F, Gallego-Giraldo L, Dixon R, Voit E . Integrative analysis of transgenic alfalfa (Medicago sativa L.) suggests new metabolic control mechanisms for monolignol biosynthesis. PLoS Comput Biol. 2011; 7(5):e1002047. PMC: 3098223. DOI: 10.1371/journal.pcbi.1002047. View

19.

Huang W, Huang L, Preston G, Naylor M, Carr J, Li Y . Quantitative in situ assay of salicylic acid in tobacco leaves using a genetically modified biosensor strain of Acinetobacter sp. ADP1. Plant J. 2006; 46(6):1073-83. DOI: 10.1111/j.1365-313X.2006.02758.x. View

20.

Chen F, Srinivasa Reddy M, Temple S, Jackson L, Shadle G, Dixon R . Multi-site genetic modulation of monolignol biosynthesis suggests new routes for formation of syringyl lignin and wall-bound ferulic acid in alfalfa (Medicago sativa L.). Plant J. 2006; 48(1):113-24. DOI: 10.1111/j.1365-313X.2006.02857.x. View