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Exploration of natural variation to understand plant adaptation to nitrogen availability

Team: Arabidopsis response to nitrogen availability

 

Objectifs et projets

Plants present a fantastic plasticity of their development in response to environmental constraints. Our approach consists in using the natural variation that exists among Arabidopsis thaliana accessions (Figure 1) to investigate the genetic components of the adaptation of plants to nitrogen limited supply - “Accessions” means “ecotypes” which are available in the Arabidopsis stock centres. For this goal, we are combining biochemical and biomolecular analyses to statistic genetics.

Acc at 0
Figure 1: Five Arabidopsis Accessions in two contrasted Nitrogen supplies (Nitrate concentration at 0.2 and 4 mM).

 

Résultats marquants

Our ultimate goal is to build « ideal plants » adapted to low nitrogen availability.

What is an “ideal plant”? It is a plant which can support growth and yield using as few nitrogen fertilizers as possible. Therefore, an ideal plant can efficiently take up nitrogen (mainly nitrate) from the soil, assimilate it and remobilize organic nitrogen with good performance. Such plants have high nitrogen use efficiency (NUE). Figure 2 shows the schematic representation of an ideal plant (Chardon et al, 2012).



Figure 2: Schematic representation of the ideal yielding plant producing a large amount of high quality grain with low fertilizer input. N uptake, N assimilation, and N recycling/remobilization efficiencies are represented with arrows.

 

How to engineer ideal plants?

The first idea is to manipulate key genes involved in NUE, such as nitrate transporter genes and genes encoding enzymes involved in nitrate reduction (NR) or amino acid synthesis (GS/GOGAT). But, since NUE is a complex trait controlled by multiple genes, it is necessary to find all the genes involved in that trait. The most accurate method is to map QTL (quantitative trait loci) with high density molecular linkage maps, in order to understand the genetic basis underlying such a complex trait (Ikram and Chardon 2010). During the past decade, we participated in the detection of many QTL involved in NUE and C/N interactions (Loudet et al 2003, Calenge et al 2006, Loudet et al 2007, Wingler et al 2010). This was achieved by using RIL (recombinant inbred lines) populations in the model plant Arabidopsis thaliana (Loudet et al, 2002).

 

Why use model plants?

Their main interest, especially for Arabidopsis, is that they show a high degree of plasticity in their development and metabolism due to natural selection pressure for adaptation to original edaphic and climatic environments. Thus, they present a large number of genotypes (referenced as “accessions” in seed stock centers) adapted to different environments, which constitute useful genetic and phenotypic resources for searchers. This is called “natural variation” and we use it to study the reaction of different genotypes face to nitrogen limitation or starvation. For example, we studied the response of 19 accessions grown in low (2mM nitrate) or high (10 mM nitrate) nitrogen supplies (Masclaux-Daubresse and Chardon, 2011). The general behavior of the plants showed the importance of key traits for NUE, particularly N remobilization which is increased at low N supply, while N uptake is favored at high N supply (Figure 3). Moreover, the variations between accessions showed that some genotypes are able to remobilize N more efficiently than others.

Figure 3
Figure 3: Schematic representation of the main characteristics at harvest of Arabidopsis plants grown with low nitrate (2 mM) and high nitrate (10 mM) supply (from Chardon et al 2012).
Means of 19 accessions of Arabidopsis and eight plant repeats are presented. Harvest Index [HI=DWSEEDS/DW(DR+SEEDS)], nitrogen harvest index [NHI=(g of N in seeds)/(g of N in the whole plant)], nitrogen remobilized harvest index [15NHI=(g of 15N in seeds)/(g of 15N in the whole plant)].


In another study, we observed the response of 22 accessions faced to N limitation or N starvation (Ikram et al, 2012) and we showed that they could be gathered in four different groups according to their growth in the different nitrogen supply conditions. Phenotypic profiling characterized four different adaptive responses, called “physiotypes”, to N limitation or starvation (Figure 4):

  • Physiotype 1 plants (Bur-0) have the best adaptation to N limitation
  • Physiotype 2 plants (Edi-0) are the most nitrogen use efficient and they are very good fighters against N starvation
  • Physiotype 3 plants (Can-0) could neither tolerate N limitation nor N starvation
  • Physiotype 4 plants (Stw-0) have N metabolism disturbed by a low N translocation to shoot

Figure 4
Figure 4: Phenotypic response profiling of representative accessions from the four classes in N limitation and N starvation (modified from Ikram et al 2012).
Individual line represents responses of each physiotype, as a percentage of the control value N+ (plain circle). The red line shows the average response of the 22 accessions. All percentages vary between –150% and +150%, except for SStarch and S/RStarch which represent a quarter of their actual percentages (asterisks).

 

How to come back to crops?

Arabidopsis behavior found with the natural variation approach allows to define ideotypes for yield and seed quality and to compare them with crop species. Figure 5 (from Chardon et al, 2012) shows the four ideotypes defined for several crops and the corresponding Arabidopsis accessions found in our previous studies.

Figure 5
Figure 5: Representation of four ideotypes summarizing the specifications of different groups using agronomic indicators (from chardon et al, 2012) such as grain yield per plant (DWSEEDS), vegetative biomass (DWVEG), total biomass at seed maturity [DW(DR+SEEDS); DR=dry remains], harvest index [HI=DWSEEDS/DW(DR+SEEDS)], nitrogen harvest index [NHI=(g of N in seeds)/(g of N in the whole plant)], utility index (UI=DWVEG/N%VEG), and the N concentration in seeds (N%SEEDS) and the whole plant at the vegetative stage (N%VEG) and at seed maturity [N%(SEEDS+DR)]. Ideotype 1 represents crops such as rice and wheat that require high grain mass, large HI and NHI, and high protein content in grain. Ideotype 2 represents high yielding crops such as corn, rapeseed, and barley, for which low N in seeds is required because it is antagonistic to starch or oil accumulation. Ideotype 3 is silage crops such as maize, for which a high vegetative biomass with a high content of proteins is demanded. Ideotype 4 represents plants that might be used for biofuel production with high total biomass at harvest and low N needs. Arabidopsis accessions matching each ideotype at low or high nitrate supplies are presented.

 

The next step

The next step of this research is to take advantage of the high throughput analysis techniques to explore natural variation in metabolome or fluxome. Thus the physiological basis of the adaptation of plants to low N availability should appear more clearly. We also investigate now the interaction between Sulphur and Nitrogen metabolisms within the BIONUT-ITN (Marie Curie Initial Training Network).
Our last approach combines statistical tools to biological analyses to test new hypotheses on NUE from a large amount of data. For example, intrigued by the numerous genes coding for similar ribosomal proteins (RP), we investigated the regulation of RP production in response to C/N status in plants by examining two independent genomic expression datasets. In response to environmental stress, plant needs to modulate its growth and development, which implies original and accurate regulation of ribosome biogenesis in each cell compartment. Ribosomes are by themselves a major proteins and nucleic acids sources in the cells. Ribosome turnover and catalytic function consumes an important part of the cell energy and nitrogen resource and we can presume that such costly machinery has to be restrained under stress conditions, especially nutrient restriction. In our work (Sormani et al., 2011), we presented a piece of evidence that specific transcriptional regulation of ribosomal protein production occurs in response to stress modifying the C/N status of plants (Figure 6).

Figure 6

Figure 6: Model of ribosome regulation by stress in plants (from Sormani et al., 2011). A. Ribosomal protein fluxes in cell of plant growing in normal condition. From the nuclear RP genes, three fluxes lead to form ribosomes and to assure high protein synthesis into the cytoplasm, mitochondrions and plastids. The diversity of cytoRP forms allows the cell to produce numerous complexes giving possibilities to produce specialized ribosomes with specialized translational activies. B. In stress condition, cell keeps only class1 RP fluxes which decrease level of translation in cytoplasm and sustains translation in mitochondrions. Cytoplasmic translational activity could be affected globally or only on a subset of mRNA. For stress affecting also plastids, cells dramatically reduce plastoRP synthesis affecting their translational activity.

 

Communications

  • S. Chaillou, F. Chardon, J. Laurette, S. Ikram, O. Loudet and F. Daniel-Vedele. Natural variation in Arabidopsis, a tool to identify genetic bases of nitrogen use efficiency. 5th International crop science congress, Che-ju, Korea April 2008 (Pdf).

  • Ikram, S., F. Chardon, F. Daniel-Vedele and S. Chaillou (2010). The natural variability of Arabidopsis thaliana, a tool to find the genetic bases of plant adaptation to nitrogen limitation. International Symposium on the Nitrogen Nutrition of Plants, Inuyama, Japon (Pdf).

  • Sormani, R., C. Masclaux-Daubresse, C. Meyer, F. Daniel-Vedele and F. Chardon (2010). Distinct transcriptional responses to stress determine ribosome composition in Arabidopsis thaliana. International Symposium on the Nitrogen Nutrition of Plants, Inuyama, Japon (Pdf).

 

Publications

IKRAM S, BEDU M, DANIEL-VEDELE FO, CHAILLOU S, CHARDON F (2012) Natural variation of Arabidopsis response to nitrogen availability. Journal of Experimental Botany 63: 91-105

CHARDON F, NOËL V, MASCLAUX-DAUBRESSE C (2012) Exploring NUE in crops and in Arabidopsis ideotypes to improve yield and seed quality. Journal of Experimental Botany 63: 3401-3412

DE PESSEMIER J, CHARDON F, JURANIEC M, DELAPLACE P, HERMANS C (2012) Natural variation of the root morphological response to nitrate supply in Arabidopsis thaliana. Mechanisms of Development "in press"

SORMANI R, MASCLAUX-DAUBRESSE C, DANIEL-VEDELE F, CHARDON F (2011) Transcriptional Regulation of Ribosome Components Are Determined by Stress According to Cellular Compartments in Arabidopsis thaliana. PLoS ONE 6: e28070

MASCLAUX-DAUBRESSE C, CHARDON F (2011) Exploring nitrogen remobilization for seed filling using natural variation in Arabidopsis thaliana. Journal of Experimental Botany 62: 2131-2142

IKRAM S, CHARDON F (2010) Plant quantitative traits. In Encyclopedia of Life Sciences (ELS). John Wiley & Sons., Chichester

CHARDON F, BARTHÉLÉMY J, DANIEL-VEDELE F, MASCLAUX-DAUBRESSE C (2010) Natural variation of nitrate uptake and nitrogen use efficiency in Arabidopsis thaliana cultivated with limiting and ample nitrogen supply. Journal of Experimental Botany 61: 2293-2302.

MASCLAUX-DAUBRESSE C, DANIEL-VEDELE F, DECHORGNAT J, CHARDON F, GAUFICHON L, SUZUKI A (2010) Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture. Annals of Botany 105: 1141-1157

WINGLER A, PURDY SJ, EDWARDS S-A, CHARDON F, MASCLAUX-DAUBRESSE C (2010) QTL analysis for sugar-regulated leaf senescence supports flowering-dependent and -independent senescence pathways. New Phytologist 185: 420-433

RICHARD-MOLARD C, KRAPP A, BRUN F, NEY B, DANIEL-VEDELE F, CHAILLOU F (2008) Plant response to nitrate starvation is determined by N storage capacity matched by nitrate uptake capacity in two Arabidopsis genotypes. J Exp Bot 59: 779-791.

LOUDET, O., V. SALIBA-COLOMBANI, C. CAMILLERI, F. CALENGE, V. GAUDON et al., (2007) Natural variation for sulfate content in Arabidopsis is highly controlled by adenosine 5'-phosphosulfate reductase. Nature Genetics 39: 896-900.

CALENGE, F., V. SALIBA-COLOMBANI, S. MAHIEU, O. LOUDET, F. DANIEL-VEDELE et al., (2006) Natural Variation for Carbohydrate Content in Arabidopsis. Interaction with Complex Traits Dissected by Quantitative Genetics. Plant Physiol. 141: 1630-1643.

LOUDET, O., S. CHAILLOU, P. MERIGOUT, J. TALBOTEC and F. DANIEL-VEDELE (2003) Quantitative Trait Loci Analysis of Nitrogen Use Efficiency in Arabidopsis. Plant Physiol. 131: 345-358.

LOUDET, O., S. CHAILLOU, A. KRAPP and F. DANIEL-VEDELE (2003) Quantitative Trait Loci Analysis of Water and Anion Contents in Interaction With Nitrogen Availability in Arabidopsis thaliana. Genetics 163: 711-722.

LOUDET, O., S. CHAILLOU, C. CAMILLERI, D. BOUCHEZ and F. DANIEL-VEDELE (2002) Bay-0 x Shahdara recombinant inbred line population: a powerful tool for the genetic dissection of complex traits in Arabidopsis. TAG 104: 1173-1184.

 

 

 

 
 

 

 

 

 
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