Effects of a barley (Hordeum vulgare) chromosome 6 grain protein content locus on whole-plant nitrogen reallocation under two different fertilisation regimes
Nancy M. Heidlebaugh A , Brian R. Trethewey A , Aravind K. Jukanti A , David L. Parrott A , John M. Martin A and Andreas M. Fischer A BA Department of Plant Sciences and Plant Pathology, Montana State University, Bozeman, MT 59717-3150, USA.
B Corresponding author. Email: fischer@montana.edu
Functional Plant Biology 35(7) 619-632 https://doi.org/10.1071/FP07247
Submitted: 24 October 2007 Accepted: 12 June 2008 Published: 21 August 2008
Abstract
A large fraction of protein N harvested with crop seeds is derived from N remobilisation from senescing vegetative plant parts, while a smaller fraction stems from de novo N assimilation occurring after anthesis. This study contrasts near-isogenic barley (Hordeum vulgare L.) germplasm, varying in the allelic state of a major grain protein content (GPC) locus on chromosome 6. Plant material was grown under both low- and high-N fertilisation levels. The analyses indicated that leaf N remobilisation occurred earlier in high-GPC germplasm under both fertilisation regimes, as indicated by an earlier decrease of total leaf N, chlorophylls, soluble- and membrane-proteins. At the same time, kernel free amino acid levels were enhanced, while leaf free amino acid levels were lower in high-GPC barleys, suggesting enhanced retranslocation of organic N to the developing sinks. Enhanced or longer availability of leaf nitrates was detected in high-GPC varieties and lines, at least under high N fertilisation, indicating that the GPC locus profoundly influences whole-plant N allocation and management. Results presented here, together with data from a recent transcriptomic analysis, make a substantial contribution to our understanding of whole-plant N storage, remobilisation and retranslocation to developing sinks.
Additional keywords: nitrogen assimilation, nitrogen remobilisation, nitrogen transport, proteolysis, senescence.
Acknowledgements
Funding for this research was provided by grants from the Montana Board of Research & Commercialisation Technology (grants #04–10 and 06–10), from the US Barley Genome Project (USDA) and from USDA-NRI (project 2005–02022) to A. M. F. Additional support from the Montana Agricultural Experiment Station is also gratefully acknowledged.
Barneix AJ
(2007) Physiology and biochemistry of source-regulated protein accumulation in the wheat grain. Journal of Plant Physiology 164, 581–590.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Close TJ,
Wanamaker SI,
Caldo RA,
Turner SM,
Ashlock DA,
Dickerson JA,
Wing RA,
Muehlbauer GJ,
Kleinhofs A, Wise RP
(2004) A new resource for cereal genomics: 22K barley GeneChip comes of age. Plant Physiology 134, 960–968.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Dembinski E,
Bany S, Raczynska-Bojanowska K
(1995) Asparagine and glutamine in the leaves of high and low protein maize. Acta Physiologiae Plantarum 17, 361–365.
Distelfeld A,
Uauy C,
Olmos S,
Schlatter AR,
Dubcovsky J, Fahima T
(2004) Microcolinearity between a 2-cM region encompassing the grain protein content locus Gpc-6B1 on wheat chromosome 6B and a 350-kb region on rice chromosome 2. Functional & Integrative Genomics 4, 59–66.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Distelfeld A,
Korol A,
Dubcovsky J,
Uauy C,
Blake T, Fahima T
(2008) Colinearity between the barley grain protein content (GPC) QTL on chromosome arm 6HS and the wheat Gpc-B1 region. Molecular Breeding , in press. ,
Feller U, Fischer A
(1994) Nitrogen metabolism in senescing leaves. Critical Reviews in Plant Sciences 13, 241–273.
| Crossref | GoogleScholarGoogle Scholar |
Hopkins M,
Taylor C,
Liu Z,
Ma F,
McNamara L,
Wang T-W, Thompson JE
(2007) Regulation and execution of molecular disassembly and catabolism during senescence. The New Phytologist 175, 201–214.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hörtensteiner S, Feller U
(2002) Nitrogen metabolism and remobilization during senescence. Journal of Experimental Botany 53, 927–937.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Jukanti AK,
Heidlebaugh NM,
Parrott DL,
Fischer IA,
McInnerney K, Fischer AM
(2008) Comparative transcriptome profiling of near-isogenic barley (Hordeum vulgare) lines differing in the allelic state of a major grain protein content locus identifies genes with possible roles in leaf senescence and nitrogen reallocation. The New Phytologist 177, 333–349.
| PubMed |
Kade M,
Barneix AJ,
Olmos S, Dubcovsky J
(2005) Nitrogen uptake and remobilization in tetraploid ‘Langdon’ durum wheat and a recombinant substitution line with the high grain protein gene Gpc-B1. Plant Breeding 124, 343–349.
| Crossref | GoogleScholarGoogle Scholar |
Krapp A, Stitt M
(1995) An evaluation of direct and indirect mechanisms for the “sink-regulation” of photosynthesis in spinach: changes in gas exchange, carbohydrates, metabolites, enzyme activities and steady-state transcript levels after cold-girdling source leaves. Planta 195, 313–323.
| Crossref | GoogleScholarGoogle Scholar |
Laemmli UK
(1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lawlor DW
(2002) Carbon and nitrogen assimilation in relation to yield: mechanisms are the key to understanding production systems. Journal of Experimental Botany 53, 773–787.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lim JD,
Cho J-I,
Park Y-I,
Hahn T-R,
Choi S-B, Jeon J-S
(2006) Sucrose transport from source to sink seeds in rice. Physiologia Plantarum 126, 572–584.
Lim PO,
Kim HJ, Nam HG
(2007) Leaf senescence. Annual Review of Plant Biology 58, 115–136.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Mickelson S,
See D,
Meyer FD,
Garner JP,
Foster CR,
Blake TK, Fischer AM
(2003) Mapping of QTL associated with nitrogen storage and remobilization in barley (Hordeum vulgare L.) leaves. Journal of Experimental Botany 54, 801–812.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Miller AJ,
Fan X,
Orsel M,
Smith SJ, Wells DM
(2007) Nitrate transport and signalling. Journal of Experimental Botany 58, 2297–2306.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Onodera Y,
Suzuki A,
Wu C-Y,
Washida H, Takaiwa F
(2001) A rice functional transcriptional activator, RISBZ1, responsible for endosperm-specific expression of storage protein genes through GCN4 motif. Journal of Biological Chemistry 276, 14139–14152.
| PubMed |
Parrott DL,
McInnerney K,
Feller U, Fischer AM
(2007) Steam-girdling of barley (Hordeum vulgare) leaves leads to carbohydrate accumulation and accelerated leaf senescence, facilitating transcriptomic analysis of senescence-associated genes. The New Phytologist 176, 56–69.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Qi JC,
Zhang GP, Zhou MX
(2006) Protein and hordein content in barley seeds as affected by nitrogen level and their relationship to beta-amylase activity. Journal of Cereal Science 43, 102–107.
| Crossref | GoogleScholarGoogle Scholar |
Roitsch T
(1999) Source-sink regulation by sugar and stress. Current Opinion in Plant Biology 2, 198–206.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
See D,
Kanazin V,
Kephart K, Blake T
(2002) Mapping genes controlling variation in barley grain protein concentration. Crop Science 42, 680–685.
Soudry E,
Ulitzur S, Gepstein S
(2005) Accumulation and remobilization of amino acids during senescence of detached and attached leaves: in planta analysis of tryptophan levels by recombinant luminescent bacteria. Journal of Experimental Botany 56, 695–702.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tang Y,
Wen X, Lu C
(2005) Differential changes in degradation of chlorophyll–protein complexes of photosystem I and photosystem II during flag leaf senescence of rice. Plant Physiology and Biochemistry 43, 193–201.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Uauy C,
Brevis JC, Dubcovsky J
(2006a) The high grain protein content gene Gpc-B1 accelerates senescence and has pleiotropic effects on protein content in wheat. Journal of Experimental Botany 57, 2785–2794.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Uauy C,
Distelfeld A,
Fahima T,
Blechl A, Dubcovsky J
(2006b) A NAC gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science 314, 1298–1301.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
von Wettstein D
(2007) From analysis of mutants to genetic engineering. Annual Review of Plant Biology 58, 1–19.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Yang L,
Mickelson S,
See D,
Blake TK, Fischer AM
(2004) Genetic analysis of the function of major leaf proteases in barley (Hordeum vulgare L.) nitrogen remobilization. Journal of Experimental Botany 55, 2607–2616.
| Crossref | GoogleScholarGoogle Scholar | PubMed |