Aphid infestation causes different changes in carbon and nitrogen allocation in alfalfa stems as well as different inhibitions of longitudinal and radial expansion

Abstract

Alfalfa (Medicago sativa) stem elongation is strongly reduced by a pea aphid (Acyrthosiphon pisum Harris) infestation. As pea aphid is a phloem feeder that does not transmit virus or toxins, assimilate withdrawal is generally considered as the main mechanism responsible for growth reduction. Using a kinematic analysis, we investigated the spatial distributions of relative elemental growth rates of control and infested alfalfa stems. The water, carbon, and nitrogen contents per unit stem length were measured along the growth zone. Deposition rates and growth-sustaining fluxes were estimated from these patterns. Severe short-term aphid infestation (200 young adults over a 24-h period) induced a strong and synchronized reduction in rates of elongation and of water and carbon deposition. Reduced nitrogen content and associated negative nitrogen deposition rates were observed in some parts of the infested stems, especially in the apex. This suggested a mobilization of nitrogen from the apical part of the growth zone, converted from a sink tissue into a source tissue by aphids. Calculation of radial growth rates suggested that aphid infestation led to a smaller reduction in radial expansion than in elongation. Together with earlier observations of long-lasting effects of a short-term infestation, this supports the hypothesis that in addition to nutrient withdrawal, a thigmomorphogenesis-like mechanism is involved in the effect of aphid infestation on stem growth.

Figure 1.

Spatial distributions of relative elemental growth rates, g(x), in alfalfa stems. A, Growth patterns before infestation in stems of control (solid line) and infested (dashed line) plants. B, Comparison of control growth at the beginning (black line) and the end (gray line) of the infestation period. C, Comparison at the end of the treatment period of control (solid line) and infested (dashed line) stems. Relative elongation rate is expressed in h⁻¹ × 1,000. Infestations were 24 h long and were carried out with 200 young prereproductive apterous adults restrained on the growth zone. In control stems, empty cages were settled on the growth zone. Data are means ± se (n = 20 for controls; n = 13 for infested).

Figure 2.

Radial relative growth along the growth zone. A, Initial diameters of controls (black solid line) and to-be-infested (black dashed line) stems before infestation, and final diameters of control (gray solid line) and infested (gray dashed line) stems at the end of infestation along the growth zone. B and C, Spatial distribution of radial relative growth rate (h⁻¹ × 1,000) of control (solid line) and infested (dashed line) stems. In B, diameters were measured directly on photographs and the precision was weak (see error bars; errors bars of control and infested treatments are superimposed). In C, radial relative growth rates were calculated using Equation 3, a and b. Data are means ± se (n = 20 for controls; n = 13 for infested).

Figure 3.

Spatial distribution of water (A), dry matter (B), carbon (C), and nitrogen (D) mass per unit stem length of control (full line) or infested (dashed line) stems. The horizontal hatched bars under the graphs represent the length of infested stem tissues. Data are means ± se (n = 20 for controls and n = 13 for infested stems).

Figure 4.

Deposition rates per unit stem length (left) or per unit stem volume (right) of water (A, A′), dry matter (B, B′), carbon (C, C′), and nitrogen (D, D′) along the growth zone of control (full line) or infested (dashed line) alfalfa stems. The horizontal hatched bars under the graphs represent the length of infested stem tissues. Data are means ± se (n = 20 for controls; n = 13 for infested).

Figure 5.

Effect of pea aphid infestation on the spatial distribution of water (A) and carbon (B) growth fluxes along the growth zone of control (solid line) or infested stems (dashed lines). Data are means ± se (n = 20 for controls; n = 13 for infested).

Figure 6.

Relationships between stem elongation rates (SER) and water flux (A) and between carbon flux (B) and water flux for both treatments (•, control stems; ○, infested stems). Data are represented on a log scale, and for each treatment orthogonal regression lines are represented. Each point represents a separate stem (n = 20 for control and n = 13 for infested stems).