The sugarcane aphid Melanaphis sacchari (Zehnter) (Hemiptera: Aphididae) has developed into a serious pest of sorghum, Sorghum bicolor (L.) Moench, in the United States (Villanueva et al. 2014, Armstrong et al. 2015, Elliott et al. 2015). Since its discovery on sorghum near Beaumont, TX, in 2013, it has rapidly spread to 17 sorghum-producing states (Bowling et al. 2016) and into Mexico (Rodríguez-del-Bosque and Teran 2015). It is believed that the sugarcane aphid shifted its host range from sugarcane, Saccharum officinarum L., to sorghum. Sugarcane aphids in the United States have been reported on sugarcane in Florida (Mead 1978) and Louisiana (White et al. 2001). In sugarcane, it is a known vector of sugarcane yellow leaf virus, causing yellow leaf disease (Singh et al. 2004, Akbar et al. 2010, Nibouche et al. 2014). The host range of this aphid pest is not limited to sorghum and sugarcane. It is also found on Johnsongrass (Sorghum halepense [L.] Pers.), Sudan grass (Sorghum bicolor subsp. drummondii [Nees ex Steud.] de Wet & Harlan), and Columbus grass (Sorghum almum Parodi) (Armstrong et al. 2015, Medina et al. 2017). Although the sugarcane aphid has been considered a serious pest of sorghum since 2013, the economic relationship of aphid densities versus yield loss have not been completely established.

Sugarcane aphids feed by sucking sap from the phloem tissue of leaves and stems. Colonies increase quickly on the abaxial surface of the leaves (Villanueva et al. 2014). Heavy infestations cause leaves to turn from yellow to brown, followed by the appearance of dark leaf surfaces covered in sooty mold growth supported by honeydew produced by the aphids (Akbar et al. 2010, Elliott et al. 2015). Honeydew-covered sorghum is a problem during harvest, as equipment may become clogged because of the sugary substance (Knutson et al. 2016, Armstrong et al. 2017). On a comparative basis under ideal environmental conditions, the reproductive rate of the sugarcane aphid is reportedly double that of the greenbug Schizaphis graminum (Rondani) on susceptible sorghum (4.45 versus 2.30 nymphs/female/d) but not significantly different on resistant sorghum (3.09 versus 2.27) (Bayoumy et al. 2015). In a more recent study, the sugarcane aphid produced 3.6 nymphs/day on susceptible sorghum Tx7000 and 1.3 nymphs/d on the resistant Tx2783 (Limaje et al. 2017), demonstrating that the sugarcane aphid has one of the fastest reproductive rates of aphids that infest grain sorghum, which must be considered when developing economic thresholds. Identification and development of sorghum germplasm resistant to the sugarcane aphid is an ongoing process. Earlier work indicates that resistant sources thus far identified in grain and forage sorghum are likely carried over from greenbug-resistant sorghums (Armstrong et al. 2015, 2017, Bayoumy et al. 2015, Limaje et al. 2017). Herein, we report host-plant evaluations using conventional screening methods in order to accelerate the development of suitable commercial sorghum lines resistant to the sugarcane aphid.

Materials and Methods

Results

From the 10 entries, excluding the known resistant Tx2783 and the susceptible Tx7000, 2 entries (OL2042 and SP7715) were considered highly resistant based on damage ratings being <3.0, whereas 4 entries (OL0029, SP74C40, SP78M30, SP73B12) exhibited resistance levels with damage scores between 3.0 and 4.0 (Table 1). The damage rating with SP7715 was identical to that of Tx2783, with a rating of 2.5, the lowest in the evaluation. However, Tx2783, SP7715, OL2042, OL0029, SP74C40, SP78M30, and SP73B12 with damage ratings between 2.5 and 3.9 did not differ statistically from those previously described. Traditionally, damage scores ≤3 have been considered highly resistant, whereas scores between 3.0 and 4.0 are considered resistant (Armstrong et al. 2015). The entries SP70B17, SP68M57, and SP6929 expressed what could be characterized as low levels of resistance, with ratings between 6.0 and 7.0, and were statistically lower than the susceptible Tx7000 and KS585 entries.

Table 1 Free-choice evaluation for sorghum germplasm infested with sugarcane aphids and evaluated for plant resistance.

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Percent chlorophyll loss, calculated from the comparison of the infested entries with noninfested entries, ranged from 96.8% for the susceptible Tx7000 to 13.8% for the SP74C40. The two lowest damage rated entries SP7715 and Tx2783 resulted in 15.2% and 15.4% losses, respectively (Table 1). Differences in plant height, where the height of the control (noninfested) was subtracted from that of the infested plants across the 20 replications, showed that the infested SP7715, OL2042, OL0029, SP74C40, SP78M30, and SP73B12 plants were, on average, 11.0 cm shorter than noninfested plants. Also, infested SP70B17, SP68M57, SP6929, and KS585 plants were, on average, 21.0 cm shorter in height than noninfested plants. The SP70B17, SP68M57, SP6929, and KS585 entries did not appear to exhibit the same degree of tolerance to sugarcane aphid feeding as the other entries previously listed.

The number of leaves on a sorghum entry can also be an indicator of sorghum susceptibility or tolerance in that sorghums exhibiting greater growth or more leaves may be less susceptible to sugarcane aphid feeding. Leaf numbers in this study ranged from 2.5 to 2.9 for the most susceptible Tx7000, SP6929, and SP70B17 entries and from 3.2 to 3.6 for the resistant Tx2783, SP7715, OL2042, OL0029, SP74C40, SP78M30, and SP73B12. Differences in plant height and the number of leaves on a sorghum entry appear to be related based on the means presented in Table 1.

There were few outliers that plotted outside the prediction intervals when chlorophyll loss was regressed against damage rating (Fig. 1), but an acceptable relationship explained the greatest portion of variation and resulted in a high correlation coefficient (R² = 0.87, P = 0.0001; Table 2). Some improvement in the model was detected when a stepwise addition for the difference in plant height was added (P = 0.0012, R² = 0.89). The next stepwise addition of the numbers of leaves on a sorghum entry did not improve the correlation coefficient (P < 0.07) as the third step in the model (Table 2).

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Table 2 Stepwise regression for the additive effects of model improvement for damage ratings (dependent variable) regressed against independent variables chlorophyll loss, difference in plant height, and number of leaves per plant.

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Discussion

The methods of evaluations in this study for sugarcane aphid–resistant sorghums emphasize the detection of tolerance as a mechanism of resistance, as opposed to the other two forms of resistance, antibiosis or antixenosis. Tolerance has been an economically important form of resistance and has often been under appreciated for its value (Reese et al. 1994). The other forms of resistance should be determined, but what was clearly shown in this evaluation is that 6 of the 10 entries, excluding the known resistant Tx2783 and susceptible Tx700, contained very good levels of host plant resistance against the sugarcane aphid. At the time of this evaluation, the six entries SP7715, OL2042, OL0029, SP74C40, SP78M30, and SP73B12 were in development, but now are commercially available.

The strong correlation coefficient for the chlorophyll loss and damage ratings has been reported by Girma et al. (1998), where they challenged susceptible and tolerant sorghums to biotype E greenbugs. In this study, we also found a strong relationship for chlorophyll loss and damage ratings, with a slight improvement when difference in plant height was added and no improvement when numbers of leaves on a plant were included in stepwise regression.

We do not know the genetic background of the resistance expressed in the sorghums evaluated, but we can assume that at least some are related to the Tx2783 background that has been documented to have both tolerance and antibiosis expressed as resistance. Tx2783 was released in 1984 with resistance to greenbug biotypes C and E (Peterson et al. 1984), and it also was found to be cross resistant to the sugarcane aphid, with expression of both tolerance and antibiosis (Armstrong et al. 2015, 2017). Greenbug-resistant sorghums that are commercially available have been invaluable in suppressing sugarcane aphid epidemics. This, in turn, has allowed for the screening and discovery of new forms of resistance that are being developed into commercial varieties.