Within-Host Multiplication and Speed of Colonization as Infection Traits Associated with Plant Virus Vertical Transmission

Abstract

Although vertical transmission from parents to offspring through seeds is an important fitness component of many plant viruses, very little is known about the factors affecting this process. Viruses reach the seed by direct invasion of the embryo and/or by infection of the ovules or the pollen. Thus, it can be expected that the efficiency of seed transmission would be determined by (i) virus within-host multiplication and movement, (ii) the ability of the virus to invade gametic tissues, (iii) plant seed production upon infection, and (iv) seed survival in the presence of the virus. However, these predictions have seldom been experimentally tested. To address this question, we challenged 18 Arabidopsis thaliana accessions with Turnip mosaic virus and Cucumber mosaic virus Using these plant-virus interactions, we analyzed the relationship between the effect of virus infection on rosette and inflorescence weights; short-, medium-, and long-term seed survival; virulence; the number of seeds produced per plant; virus within-host speed of movement; virus accumulation in the rosette and inflorescence; and efficiency of seed transmission measured as a percentage and as the total number of infected seeds. Our results indicate that the best estimators of percent seed transmission are the within-host speed of movement and multiplication in the inflorescence. Together with these two infection traits, virulence and the number of seeds produced per infected plant were also associated with the number of infected seeds. Our results provide support for theoretical predictions and contribute to an understanding of the determinants of a process central to plant-virus interactions.IMPORTANCE One of the major factors contributing to plant virus long-distance dispersal is the global trade of seeds. This is because more than 25% of plant viruses can infect seeds, which are the main mode of germplasm exchange/storage, and start new epidemics in areas where they were not previously present. Despite the relevance of this process for virus epidemiology and disease emergence, the infection traits associated with the efficiency of virus seed transmission are largely unknown. Using turnip mosaic and cucumber mosaic viruses and their natural host Arabidopsis thaliana as model systems, we have identified the within-host speed of virus colonization and multiplication in the reproductive structures as the main determinants of the efficiency of seed transmission. These results contribute to shedding light on the mechanisms by which plant viruses disperse and optimize their fitness and may help in the design of more-efficient strategies to prevent seed infection.

Keywords: Arabidopsis thaliana; cucumber mosaic virus; seed transmission; turnip mosaic virus; vertical transmission; virulence; virus multiplication; within-host movement.

FIG 1

Virus seed transmission in Arabidopsis. TuMV seed transmission percentage (A) and log number of infected seeds (B) and CMV seed transmission percentage (C) and log number of infected seeds (D) in 18 Arabidopsis accessions are shown. Data for JPN1-TuMV (black), UK1-TuMV (gray), De72-CMV (red), Fny-CMV (blue), and LS-CMV (green) are represented. Note the different scale of each panel.

FIG 2

Bivariate relationships between percent virus seed transmission and infection traits. Regressions considering data for both viruses together (A and B), only JPN1-TuMV (C to E), and only Fny-CMV (F to H) are shown. Linear relationships of percent virus seed transmission and speed of virus movement in centimeters per day (purple), virus multiplication in the inflorescence in nanograms of viral RNA per microgram of total RNA (orange), virulence as 1 − (SW_i/SW_m) (light blue), and long-term seed survival as G_48i/G_48m (green) are represented.

FIG 3

Bivariate relationships between the number of virus-infected seeds and infection traits. Regressions considering data for both viruses together (A to C), only JPN1-TuMV (D to F), and only Fny-CMV (G to I) are shown. Linear relationships of the log number of virus-infected seeds and percent virus seed transmission (brown), virulence as 1 − (SW_i/SW_m) (light blue), virus multiplication in the inflorescence in nanograms of viral RNA per microgram of total RNA (orange), and log number of seeds per infected plant (dark blue) are represented.

FIG 4

Bivariate relationships between the main predictors of the number of virus-infected seeds. Regressions considering data for both viruses together (A and B), only JPN1-TuMV (C and D), and only Fny-CMV (E and F) are shown. Linear relationships of percent infected seeds and log number of seeds per infected plant (dark blue) and of percent infected seeds and virulence as 1 − (SW_i/SW_m) (light blue) are represented.

FIG 5

Association between experimental and estimated virus seed transmission of 5 TuMV and CMV isolates in 18 Arabidopsis accessions. Correlations between estimated values of percent TuMV seed transmission derived from the TuMV-specific model (A) and from the global model (B), percent CMV seed transmission derived from the CMV-specific model (C) and from the global model (D), the log number of TuMV-infected seeds derived from the TuMV-specific models (E) and from the global model (F), and the log number of CMV-infected seeds derived from the CMV-specific models (G) and from the global model (H) and the corresponding experimental values are shown. Data for UK1-TuMV (gray), JPN1-TuMV (black), LS-CMV (green), Fny-CMV (blue), and De72-CMV (red) are represented. Note the different scale of each panel.

FIG 6

Association between experimental and estimated virus seed transmission of the 2 TuMV and 3 CMV isolates in 18 Arabidopsis accessions. (A to D) Correlations of percent TuMV seed transmission derived from the TuMV-specific model (A and B) and from the global model (C and D) to the corresponding experimental values. (E to J) Correlations of percent CMV seed transmission derived from the CMV-specific model (E to G) and from the global model (H to J) to the corresponding experimental values. Data for JPN1-TuMV (black), UK1-TuMV (gray), LS-CMV (green), Fny-CMV (blue), and De72-CMV (red) are represented.

FIG 7

Association between experimental and estimated virus seed transmission of the 2 TuMV and 3 CMV isolates in 18 Arabidopsis accessions. (A to D) Correlations of the number of TuMV-infected seeds derived from the TuMV-specific model (A and B) and from the global model (C and D) to the corresponding experimental values. (E to J) Correlations of the number of CMV-infected seeds derived from the CMV-specific model (E to G) and from the global model (H to J) to the corresponding experimental values. Data for JPN1-TuMV (black), UK1-TuMV (gray), LS-CMV (green), Fny-CMV (blue), and De72-CMV (red) are represented.