Characterization ofdrr1, an Alkamide-Resistant Mutant of Arabidopsis, Reveals an Important Role for Small Lipid Amides in Lateral Root Development and Plant Senescence

Abstract

Alkamides belong to a class of small lipid signals of wide distribution in plants, which are structurally related to the bacterial quorum-sensing signals N-acyl-L-homoserine lactones. Arabidopsis (Arabidopsis thaliana) seedlings display a number of root developmental responses to alkamides, including primary root growth inhibition and greater formation of lateral roots. To gain insight into the regulatory mechanisms by which these compounds alter plant development, we performed a mutant screen for identifying Arabidopsis mutants that fail to inhibit primary root growth when grown under a high concentration of N-isobutyl decanamide. A recessive N-isobutyl decanamide-resistant mutant (decanamide resistant root [drr1]) was isolated because of its continued primary root growth and reduced lateral root formation in response to this alkamide. Detailed characterization of lateral root primordia development in the wild type and drr1 mutants revealed that DRR1 is required at an early stage of pericycle cell activation to form lateral root primordia in response to both N-isobutyl decanamide and N-decanoyl-Lhomoserine lactone, a highly active bacterial quorum-sensing signal. Exogenously supplied auxin similarly inhibited primary root growth and promoted lateral root formation in wild-type and drr1 seedlings, suggesting that alkamides and auxin act by different mechanisms to alter root system architecture. When grown both in vitro and in soil, drr1 mutants showed dramatically increased longevity and reduced hormone-and age-dependent senescence, which were related to reduced lateral root formation when exposed to stimulatory concentrations of jasmonic acid. Taken together, our results provide genetic evidence indicating that alkamides and N-acyl-L-homoserine lactones can be perceived by plants to modulate root architecture and senescence-related processes possibly by interacting with jasmonic acid signaling.

N-3-Oxo-Decanoyl-l-Homoserine-Lactone Activates Auxin-Induced Adventitious Root Formation via Hydrogen Peroxide- and Nitric Oxide-Dependent Cyclic GMP Signaling in Mung Bean

“…Alteration of root development by AHLs or plant growth-promoting rhizobacteria involves jasmonate, ethylene, and salicylic acid signaling pathways (Méndez-Bravo et al, 2010;Morquecho-Contreras et al, 2010;Shi et al, 2010). Here, we found that 3-O-C10-HL still retained the partial ability to promote adventitious root formation even in the presence of the auxin transport inhibitor NPA, indicating that auxin-independent signaling should not be excluded and may participate in 3-O-C10-HL-induced adventitious root formation.…”

“…Previous studies showed that modulating Arabidopsis primary and lateral root formation by some AHLs or alkamide, particularly those AHLs with an unmodified branched chain, is independent of auxin signaling (Ortíz-Castro et al, 2008;Méndez-Bravo et al, 2010;Morquecho-Contreras et al, 2010). For example, C10-HL treatment was unable to enhance GUS activity in Arabidopsis transgenic seedlings harboring the auxinresponse DR5:uidA gene construct (Ortíz-Castro et al, 2008).…”

“…Recently, more evidence demonstrate that AHLs are able to modulate plant growth and development (Mathesius et al, 2003;Ortíz-Castro et al, 2008;von Rad et al, 2008;Méndez-Bravo et al, 2010;MorquechoContreras et al, 2010). In Arabidopsis, treatment with AHLs alters primary growth, lateral root formation, and root hair development; specifically, AHLs with different lengths of unmodified branched chains differentially affect the root architecture.…”

“…S2A). Previous reports showed that the ethylene, salicylic acid, or jasmonic acid signaling pathways are involved in plant responses to AHLs or plant growth-promoting rhizobacteria stimulation (Morquecho-Contreras et al, 2010;Shi et al, 2010). We used the ethylene action inhibitor AgNO 3 , the salicylic acid synthesis inhibitor paclobutrazol, and the jasmonic acid synthesis inhibitor diethyldithiocarbamic acid to determine their roles in our system.…”

“…Recent evidence indicates that plants are able to perceive AHLs; the application of AHLs to Arabidopsis or Medicago truncatula results in distinct transcriptional changes in the roots and shoots and affects primary root growth, lateral root formation, and root hair development (Mathesius et al, 2003;Ortíz-Castro et al, 2008;von Rad et al, 2008;Morquecho-Contreras et al, 2010). Similar to the structure of AHLs, the fatty acid amides, including N-acyl-ethanolamines (NAEs) and alkamides in plants, are also capable of regulating root and shoot architecture (Laxalt and Munnik, 2002;Campos-Cuevas et al, 2008;Morquecho-Contreras et al, 2010), and the Arabidopsis recessive mutant decanamide-resistant root1 (drr1) was isolated based on its continuous primary root and reduced lateral root formation in response to decanamide (an alkamide) or AHLs (Morquecho-Contreras et al, 2010). Further analysis demonstrated that DRR1 is required in the early stage of pericycle cell activation to form lateral root primordia, suggesting that plants may share a common pathway to perceive NAEs and AHLs for root development.…”