Evidence of a role for foliar salicylic acid in regulating the rate of post-ingestive protein breakdown in ruminants and contributing to landscape pollution

A. H. Kingston-Smith; T. E. Davies; J. E. Edwards; A. Gay; L. A. J. Mur

doi:10.1093/jxb/ers048

Evidence of a role for foliar salicylic acid in regulating the rate of post-ingestive protein breakdown in ruminants and contributing to landscape pollution

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Evidence of a role for foliar salicylic acid in regulating the rate of post-ingestive protein breakdown in ruminants and contributing to landscape pollution. / Kingston-Smith, A. H.; Davies, T. E.; Edwards, J. E. et al.

In: Journal of Experimental Botany, Vol. 63, No. 8, 09.02.2012, p. 3243-3255.

Research output: Contribution to journal › Article › peer-review

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@article{20ee8542fd574f7c8e7738b9e3dfab6a,

title = "Evidence of a role for foliar salicylic acid in regulating the rate of post-ingestive protein breakdown in ruminants and contributing to landscape pollution",

abstract = "Ruminant farming is important to global food security, but excessive proteolysis in the rumen causes inefficient use of nitrogenous plant constituents and environmental pollution. While both plant and microbial proteases contribute to ruminal proteolysis, little is known about post-ingestion regulation of plant proteases except that activity in the first few hours after ingestion of fresh forage can result in significant degradation of foliar protein. As the signal salicylic acid (SA) influences cell death during both biotic and abiotic stresses, Arabidopsis wild-type and mutants were used to test the effect of SA on proteolysis induced by rumen conditions (39 degrees C and anaerobic in a neutral pH). In leaves of Col-0, SA accumulation was induced by exposure to a rumen microbial inoculum. Use of Arabidopsis mutants with altered endogenous SA concentrations revealed a clear correlation with the rate of stress-induced proteolysis; rapid proteolysis occurred in leaves of SA-accumulating mutants cpr5-1 and dnd1-1 whereas there was little or no proteolysis in sid2-1 which is unable to synthesize SA. Reduced proteolysis in npr1-1 (Non-expressor of Pathogenesis Related genes) demonstrated a dependence on SA signalling. Slowed proteolysis in sid2-1 and npr1-1 was associated with the absence of a 34.6 kDa cysteine protease. These data suggest that proteolysis in leaves ingested by ruminants is modulated by SA. It is therefore suggested that influencing SA effects in planta could enable the development of forage crops with lower environmental impact and increased production potential.",

keywords = "Arabidopsis thaliana, cell signalling, environment, proteolysis, ruminants, salicylic acid",

author = "Kingston-Smith, {A. H.} and Davies, {T. E.} and Edwards, {J. E.} and A. Gay and Mur, {L. A. J.}",

note = "Online early; open access RONO: 03135-CGC ",

year = "2012",

month = feb,

day = "9",

doi = "10.1093/jxb/ers048",

language = "English",

volume = "63",

pages = "3243--3255",

journal = "Journal of Experimental Botany",

issn = "0022-0957",

publisher = "Oxford University Press",

number = "8",

}

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TY - JOUR

T1 - Evidence of a role for foliar salicylic acid in regulating the rate of post-ingestive protein breakdown in ruminants and contributing to landscape pollution

AU - Kingston-Smith, A. H.

AU - Davies, T. E.

AU - Edwards, J. E.

AU - Gay, A.

AU - Mur, L. A. J.

N1 - Online early; open access RONO: 03135-CGC

PY - 2012/2/9

Y1 - 2012/2/9

N2 - Ruminant farming is important to global food security, but excessive proteolysis in the rumen causes inefficient use of nitrogenous plant constituents and environmental pollution. While both plant and microbial proteases contribute to ruminal proteolysis, little is known about post-ingestion regulation of plant proteases except that activity in the first few hours after ingestion of fresh forage can result in significant degradation of foliar protein. As the signal salicylic acid (SA) influences cell death during both biotic and abiotic stresses, Arabidopsis wild-type and mutants were used to test the effect of SA on proteolysis induced by rumen conditions (39 degrees C and anaerobic in a neutral pH). In leaves of Col-0, SA accumulation was induced by exposure to a rumen microbial inoculum. Use of Arabidopsis mutants with altered endogenous SA concentrations revealed a clear correlation with the rate of stress-induced proteolysis; rapid proteolysis occurred in leaves of SA-accumulating mutants cpr5-1 and dnd1-1 whereas there was little or no proteolysis in sid2-1 which is unable to synthesize SA. Reduced proteolysis in npr1-1 (Non-expressor of Pathogenesis Related genes) demonstrated a dependence on SA signalling. Slowed proteolysis in sid2-1 and npr1-1 was associated with the absence of a 34.6 kDa cysteine protease. These data suggest that proteolysis in leaves ingested by ruminants is modulated by SA. It is therefore suggested that influencing SA effects in planta could enable the development of forage crops with lower environmental impact and increased production potential.

AB - Ruminant farming is important to global food security, but excessive proteolysis in the rumen causes inefficient use of nitrogenous plant constituents and environmental pollution. While both plant and microbial proteases contribute to ruminal proteolysis, little is known about post-ingestion regulation of plant proteases except that activity in the first few hours after ingestion of fresh forage can result in significant degradation of foliar protein. As the signal salicylic acid (SA) influences cell death during both biotic and abiotic stresses, Arabidopsis wild-type and mutants were used to test the effect of SA on proteolysis induced by rumen conditions (39 degrees C and anaerobic in a neutral pH). In leaves of Col-0, SA accumulation was induced by exposure to a rumen microbial inoculum. Use of Arabidopsis mutants with altered endogenous SA concentrations revealed a clear correlation with the rate of stress-induced proteolysis; rapid proteolysis occurred in leaves of SA-accumulating mutants cpr5-1 and dnd1-1 whereas there was little or no proteolysis in sid2-1 which is unable to synthesize SA. Reduced proteolysis in npr1-1 (Non-expressor of Pathogenesis Related genes) demonstrated a dependence on SA signalling. Slowed proteolysis in sid2-1 and npr1-1 was associated with the absence of a 34.6 kDa cysteine protease. These data suggest that proteolysis in leaves ingested by ruminants is modulated by SA. It is therefore suggested that influencing SA effects in planta could enable the development of forage crops with lower environmental impact and increased production potential.

KW - Arabidopsis thaliana

KW - cell signalling

KW - environment

KW - proteolysis

KW - ruminants

KW - salicylic acid

UR - http://hdl.handle.net/2160/8128

U2 - 10.1093/jxb/ers048

DO - 10.1093/jxb/ers048

M3 - Article

C2 - 22378947

VL - 63