SLI1 confers broad‐spectrum resistance to phloem‐feeding insects

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.

Effects of condensed tannins on behavior and performance of a specialist aphid on aspen

“…Defence response genes in aspen are polymorphic (García & Ingvarsson, 2007 ; Wang et al, 2016a , 2016b , 2020 ) suggestively crafted by extended and complex balancing selective processes (Delph & Kelly, 2013 ; Hurst, 2009 ), and co‐evolution between aphids and their hosts is indeed likely to be an ongoing process that continuously and simultaneously reshapes plants' defensive traits and mechanisms that enable aphids to cope with those traits (Cope et al, 2021 ; Züst & Agrawal, 2016 ). In addition, several piercing‐sucking arthropods live on aspen, including leafhoppers, eriophyid mites, and leaf‐galling aphids of the Pemphiginae (Robinson et al, 2012 ), and resistance might not only protect against piercing damage by one aphid species but against an entire feeding guild as suggested for several plant systems (Kloth et al, 2021 ; Ng & Perry, 2004 ; Nombela et al, 2003 ; von Bargen et al, 2020 ). Thus, the varied impact of environmental and ontogenetic status on resistance and growth is an expected outcome of balancing selection.…”

“…Many kinds of aphid feeding deterrents and barriers have been reported in the literature, including high secondary metabolite contents in sap (Jakobs et al, 2019 ), sieve element occlusion (Will et al, 2013 ), and structural barriers (Kloth et al, 2021 ). Moreover, aphids are masters of manipulation that not only release effectors that help them to overcome local host defences (Züst & Agrawal, 2016 ) but also construct niches of their own by changing their host's metabolism (Jakobs et al, 2019 ).…”

“…An aphid was placed on the adaxial side of a mature fully expanded leaf (number 7–10 from the top) of each of these plants with a 1‐ to 2‐cm‐long, 18‐μm‐diameter gold wire glued to its dorsum. The other end of the wire was connected to a Giga 8d DC amplifier (EPG systems, 2021 ), and linked to a computer to capture and store the EPG‐generated waveforms for later interpretation (Kloth et al, 2021 ; ten Broeke et al, 2013 ). Stylet+d and Stylet+a software packages provided by EPG systems ( 2021 ) were used to record and annotate the EPG waveforms (Appendix, Figure S3 ).…”

“…Stylet+d and Stylet+a software packages provided by EPG systems ( 2021 ) were used to record and annotate the EPG waveforms (Appendix, Figure S3 ). Behavioral variables, listed in Table 1 , were calculated using R v. 4.0.4 software (R Core Team, 2020 ), and the procedure presented by Kloth et al ( 2021 ), except that waveforms that did not occur were assigned zero values for duration measurements, missing values for calculating mean values, and total durations for latency times (i.e., the time from the start of a recording until the start of another behavior). Behaviors that were ongoing at the end of a recording session (after 8 h) were included in their short, truncated form.…”

Identification of new proteins in mature sieve elements

“…We identified a previously undescribed HSP20L family protein in root sieve elements. Two other sieve element proteins from the same family, SLI1 and RTM2, are involved in defense processes against aphids and viruses, respectively (Chisholm et al, 2001; Kloth et al, 2017; Kloth et al, 2021). The molecular mechanisms behind the HSP20L resistances are poorly understood (Kloth & Kormelink, 2020).…”