Developmental genes have pleiotropic effects on plant morphology and source capacity, eventually impacting on seed protein content and productivity in pea

Abstract

Increasing pea (Pisum sativum) seed nutritional value and particularly seed protein content, while maintaining yield, is an important challenge for further development of this crop. Seed protein content and yield are complex and unstable traits, integrating all the processes occurring during the plant life cycle. During filling, seeds are the main sink to which assimilates are preferentially allocated at the expense of vegetative organs. Nitrogen seed demand is satisfied partly by nitrogen acquired by the roots, but also by nitrogen remobilized from vegetative organs. In this study, we evaluated the respective roles of nitrogen source capacity and sink strength in the genetic variability of seed protein content and yield. We showed in eight genotypes of diverse origins that both the maximal rate of nitrogen accumulation in the seeds and nitrogen source capacity varied among genotypes. Then, to identify the genetic factors responsible for seed protein content and yield variation, we searched for quantitative trait loci (QTL) for seed traits and for indicators of sink strength and source nitrogen capacity. We detected 261 QTL across five environments for all traits measured. Most QTL for seed and plant traits mapped in clusters, raising the possibility of common underlying processes and candidate genes. In most environments, the genes Le and Afila, which control internode length and the switch between leaflets and tendrils, respectively, determined plant nitrogen status. Depending on the environment, these genes were linked to QTL of seed protein content and yield, suggesting that source-sink adjustments depend on growing conditions.

Figure 1.

Seed weight (A) and seed protein content (B) of eight genotypes measured in three different conditions: plants were grown in glasshouse and all pods, except those on the second-flowering node, were removed (depodding treatment), control plants grown in glasshouse, and control plants grown in field trials.

Figure 2.

Frequency distribution of the seed protein content, seed weight, seed number, and seed yield of the ‘Térèse’ × K586 recombinant inbred population in the five field trials: n = 2; Dijon, France (2000) one-row trial, D00row; Dijon, France (2002) one-row trial, D02row; Dijon, France (2002) plot trial, D02plot; Chartainvilliers, France (2000) one-row trial, C00row; Premesques, France (2000) one-row trial, P00row. The arrowheads indicate the mean value of the parental lines. K, K586; T, ‘Térèse’.

Figure 3.

CIs of QTL detected by composite interval mapping for all traits in five field trials. For each QTL, the names of the variable and of the trial are indicated. Dotted lines indicate seed trait QTL (Seed N, Seed Y, 1-seed W, Seed PC, NcotCel, and VcotCel), full lines indicate phenology and morphology trait QTLs (BegFlo, EndFlo, Harvest, Height, NBranch); dashed lines indicate source capacity QTL (DMBSF, %NBSF, DMstraw, %Nstraw; QNBSF, QNmob, and QNacc; NNI); dashed and dotted lines indicate QTL of indicators of assimilate allocation (HI and NHI). Field trials: Dijon, France (2000) one-row trial, D00row; Dijon, France (2002) one-row trial, D02row; Dijon, France (2002) plot trial, D02plot; Chartainvilliers, France (2000) one-row trial, C00row; Premesques, France (2000) one-row trial, P00row. Arrowheads indicate the Af, Le, and Rms6 loci.

Figure 3.

CIs of QTL detected by composite interval mapping for all traits in five field trials. For each QTL, the names of the variable and of the trial are indicated. Dotted lines indicate seed trait QTL (Seed N, Seed Y, 1-seed W, Seed PC, NcotCel, and VcotCel), full lines indicate phenology and morphology trait QTLs (BegFlo, EndFlo, Harvest, Height, NBranch); dashed lines indicate source capacity QTL (DMBSF, %NBSF, DMstraw, %Nstraw; QNBSF, QNmob, and QNacc; NNI); dashed and dotted lines indicate QTL of indicators of assimilate allocation (HI and NHI). Field trials: Dijon, France (2000) one-row trial, D00row; Dijon, France (2002) one-row trial, D02row; Dijon, France (2002) plot trial, D02plot; Chartainvilliers, France (2000) one-row trial, C00row; Premesques, France (2000) one-row trial, P00row. Arrowheads indicate the Af, Le, and Rms6 loci.

Figure 4.

Relationship between plant nitrogen content and plant biomass at BSF in the RIL1 population. Different allelic combinations at Le and Af genes are indicated. A, Dijon, France (2000) one-row field trial. Plant biomass is expressed in grams/plant. B, Dijon, France (2002) plot trial. Plant biomass is expressed in g/0.15 m² square. In this trial, Ncrit was calculated.