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. 2021 Aug;44(8):2765-2776.
doi: 10.1111/pce.14064. Epub 2021 May 5.

SLI1 confers broad-spectrum resistance to phloem-feeding insects

Karen J Kloth  1 , Parth Shah  1 , Colette Broekgaarden  2 , Cecilia Ström  3 , Benedicte R Albrectsen  3 , Marcel Dicke  1
Affiliations

SLI1 confers broad-spectrum resistance to phloem-feeding insects

Karen J Kloth et al. Plant Cell Environ. 2021 Aug.

Abstract

Resistance (R) genes usually compete in a coevolutionary arms race with reciprocal effectors to confer strain-specific resistance to pathogens or herbivorous insects. Here, we investigate the specificity of SLI1, a recently identified R gene in Arabidopsis that encodes a small heat shock-like protein involved in resistance to Myzus persicae aphids. In a panel with several aphid and whitefly species, SLI1 compromised reproductive rates of three species: the tobacco aphid M. persicae nicotianae, the cabbage aphid Brevicoryne brassicae and the cabbage whitefly Aleyrodes proletella. Electrical penetration graph recording of aphid behaviour, revealed shorter salivations and a 3-to-5-fold increase in phloem feeding on sli1 loss-of-function plants. The mustard aphid Lipaphis erysimi and Bemisia tabaci whitefly were not affected by SLI1. Unlike the other two aphid species, L. erysimi exhibited repetitive salivations preceding successful phloem feeding, indicating a role of salivary effectors in overcoming SLI1-mediated resistance. Microscopic characterization showed that SLI1 proteins localize in the sieve tubes of virtually all above- and below-ground tissues and co-localize with the aphid stylet tip after penetration of the sieve element plasma membrane. These observations reveal an unconventional R gene that escapes the paradigm of strain specificity and confers broad-spectrum quantitative resistance to phloem-feeding insects.

Keywords: R genes; aphids; phloem; plant resistance; whiteflies.

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Conflict of interest statement

The authors have no conflicts of interest to declare.

Figures

FIGURE 1
FIGURE 1
Aphid and whitefly performance on Col‐0 and sli1‐1 and sli1‐2 mutants. (a) Number of offspring per adult aphid of Myzus persicae nicotiana (Mpn), Brevicoryne brassicae (Bb) and Lipaphis erysimi (Le) and number of eggs per adult whitefly per day of Aleyrodes proletella (Ap) and Bemisia tabaci (Bt) (days post‐infestation: 14 days (M. persicae nicotianae and B. brassicae), 10 days (L .erysimi), 7 days (A. proletella), and 5 days (B. tabaci)). (b) Aphid development time from neonate to first reproduction. (c). Founder aphids lost to dispersal or mortality. (d) Mortality of whiteflies (* p < .05, ** p < .01, *** p < .001, one‐way ANOVA tests (reproductive rates), Kruskal Wallis tests (developmental time and mortality) and χ 2 tests (lost aphids), violin plots show interquartile range with kernel density distribution and median value (horizontal line), dots represent observations, in order of plant material (Col‐0, sli1‐1, sli1‐2): Mpn n = 20, 21, 21; Bb n = 18, 21, 21; Le n = 20, 17, 22; Ap n = 15, 15, 15; and Bt n = 10, 10, 10, insect photo's courtesy of Hans Smid)
FIGURE 2
FIGURE 2
Phloem feeding by Myzus persicae nicotianae, Brevicoryne brassicae and Lipaphis erysimi on sli1‐1 and sli1‐2 knockout mutants and the Col‐0 wild type as percentage of total time (mean values with SE in shaded area, n = 15) [Colour figure can be viewed at wileyonlinelibrary.com]
FIGURE 3
FIGURE 3
Repetitive potential drops and the effects on phloem feeding on Col‐0. (a) ‘Normal’ potential drop (pd) and (b) repetitive potential drop (R‐pd) of Lipaphis erysimi. (c) Electropenetrographs from Myzus persicae nicotianae (upper), Brevicoryne brassicae (middle), and L. erysimi aphids (lower) on Col‐0. After the start of probing (black triangle), aphids penetrated the cell wall matrix and occasionally showed punctures of cell membranes (pd's) followed by a approximately 5 s intracellular phase (pathway phase, red boxplots). Only L. erysimi showed repetitive potential drops (R‐pd's) with a long, approximately 20 s, intracellular phase (blue boxplot). When the phloem was reached, aphids secreted watery saliva (not shown in boxplot) and started phloem feeding (yellow boxplots). Lipaphis erysimi required two‐fold more time to reach the phloem phase than the other two aphid species (p = .0087) but fed longer from the phloem (p = .000, linear mixed model with aphid/plant individual as random effect, probes as biological replicates, including only those probing events with the following sequence of events: non‐probing > pathway > (repetitive potential drops >) phloem salivation > phloem feeding; M. persicae nicotianae n = 35 probes (14 aphids), B. brassicae n = 18 probes (10 aphids), L. erysimi n = 14 probes (10 aphids)). Boxplots represent median (thick line), interquartile range (box), 1.5‐fold interquartile range (whiskers) and extremes (open circles) [Colour figure can be viewed at wileyonlinelibrary.com]
FIGURE 4
FIGURE 4
Localization of SLI1 proteins and Myzus persicae aphid stylets in Arabidopsis. YFP fusion proteins of SLI1 (in green) expressed under the native promoter in: (a) the petiole of a mature leaf, (b) the inflorescence stem, (c) the growth apex, and (d) the root tip. Cryofixation of aphid stylets in a mature leaf with: (e) upper part of stylets, (f) the stylet tip with maxillary stylets protruding into a sieve tube, and (g) co‐localization of the stylet tip with SLI1 proteins (green = pSLI1:YFP:SLI1, magenta = chlorophyll (a–c, e), Mitotracker Deep Red (d), s = stylets, arrow = sieve tube, images (a–e) and (g) confocal laser scanning microscopy, image (f) light microscopy, scale bars (a) 20 μm, (b) 250 μm, (c, d) 50 μm, (e) 25 μm, (f‐g) 5 μm) [Colour figure can be viewed at wileyonlinelibrary.com]
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