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Influence of Cytoplasmic Male-sterility on the Expression of Resistance to Insects in Sorghum

H.C. Sharma1, Mukesh K Dhillon1, Jagdish S Naresh2, Ram Singh2, G Pampapathy1 and B.V.S. Reddy1

1International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Patancheru 502 324, Andhra Pradesh, India. E-mail: h.sharma@cgiar.org; g.pampapathy@cgiar.org
2
CSS Haryana Agricultural University, Hisar, Haryana, India. mukeshdhillon@rediffmail.com

Abstract

Cytoplasmic nuclear male-sterility has been used widely in a large number of crops to exploit the heterotic potential for increasing their productivity. Use of a limited number of male-sterility sources usually results in narrowing the genetic base, and thus, increasing the vulnerability of crops to various biotic and abiotic stresses. We examined the influence of cytoplasmic nuclear male-sterility on expression of resistance to insects in sorghum (Sorghum bicolor), and developed strategies for deploying insect-resistance genes through high-yielding hybrids for integrated pest management. A diverse range of male-sterile, maintainer, and pollinator lines were evaluated for their resistance to sorghum shoot fly (Atherigona soccata), aphid (Melanaphis sacchari), shoot bug (Peregrinus maidis), and sorghum midge (Stenodiplosis sorghicola) under natural and/or artificial infestation. In general, the CMS lines were significantly more susceptible to insects than their maintainer lines. The male-sterile lines of the insect-resistant seed parents were as susceptible as the male-sterile or maintainer lines of the susceptible seed parents, suggesting that the maintainer lines contain factors that influence expression of resistance to insects. Resistance to insects seems to be influenced by the interaction of factors in the cytoplasm of the maintainer lines with the nuclear genes. To develop insect-resistant hybrids, resistance is needed in both the parents. Therefore, there is a need to transfer the insect resistance gene(s) in to both the parents.

Media summary

Some cytoplasmic factors present in the cytoplasmic nuclear male-sterile lines influence the expression of resistance to insects. To develop insect resistant hybrids in sorghum, resistance is needed in both the parents. Deployment of insect-resistant hybrid cultivars will reduce the vulnerability of crop to pest outbreaks, minimize pesticide use, conserve natural enemies, and protect the environment.

Keywords

sorghum, host-plant resistance, shoot fly, aphid, shoot bug, midge.

Introduction

Cytoplasmic nuclear male-sterility (CMS) has been used on large-scale for exploiting heterotic potential for increasing crop production (Kaul 1988). Large-scale use of such cultivars if based on a single source of cytoplasm may render the entire crop vulnerable to outbreaks of insect pests and diseases (Yang et al. 1989). In addition to diversifying CMS sources, it is important to understand the interactions between insect pests and hybrid parents to develop appropriate strategies for the development and deployment of insect-resistant hybrids. Therefore, we examined the influence of cytoplasmic nuclear male-sterility on expression of resistance to major insects in sorghum, and developed strategies for deploying insect-resistance genes through high-yielding hybrids for integrated pest management.

Methods

The present studies were undertaken on a diverse range of male-sterile, maintainer, and pollinator lines to understand the influence of cytoplasmic male-sterility on expression of resistance to sorghum shoot fly (Atherigona soccata), shoot bug (Peregrinus maidis), yellow sugarcane aphid (Melanaphis sacchari), and sorghum midge (Stenodiplosis sorghicola). The material was evaluated for resistance/susceptibility to insects under natural and/or artificial infestation. The material was planted in the field in two rows each 2m long, and 75 cm apart. The seedlings were thinned to a spacing of 15 cm between the plants 10 days after emergence. There were three replications in a randomized complete block design. Normal agronomic practices were followed for raising the crop, but no insecticide was applied. Twelve A and B pairs were evaluated for resistance to shoot fly, stem borer, and shoot bug; while 35 pairs were evaluated for resistance to yellow sugarcane aphid, and four pairs for resistance to sorghum midge. Data were recorded on percentage plants with shoot fly deadhearts at 14 days after seedling emergence (Sharma et al. 1992). Shoot bug and aphid damage were recorded visually on a 1 to 9 damage rating scale (1 = <10% leaf area damaged, and 9 = >80% leaf area damaged) (Sharma et al. 1997). Resistance to sorghum midge was measured in terms of number of midges emerged per panicle when infested with 40 midge females for 2 consecutive days at the flowering stage using a headcage technique (Sharma et al. 1988). Dataoninsect damage and/or numbers was subjected to analysis of variance.

Results

The deadheart formation due to shoot fly damage was 75.7% in the male-sterile lines and 68.6% in the maintainer lines across 12 pairs tested (Fig. 1a). However, mean deadheart formation in the shoot fly-resistant and susceptible CMS and their maintainer was 64.8 versus 86.6%, and 49.5 versus 88.1%, respectively. In case of shoot bug, P. maidis, the CMS lines showed a damage rating of 7.0 compared to 7.4 for the maintainer lines (Fig. 1b).

Fig. 1. Effect of cytoplasmic male-sterility on expression of resistance to insects. a – shoot fly, Atherigona soccata, b: shoot bug, Peregrinus maidis, c: yellow sugarcane aphid, Melanaphis sacchari, and d: sorghum midge, Stenodiplosis sorghicola. Overall = Mean insect infestation/numbers across CMS (A) and their maintainer (B) lines tested. Resistant = Mean insect infestation/numbers in the insect-resistant CMS and maintainer lines, and Susceptible = Mean insect infestation/numbers in the insect-susceptible CMS and maintainer lines tested.

The shoot bug-resistant parents suffered a damage rating of 6.7 in the CMS lines and 5.4 in the maintainer lines; while the shoot bug-susceptible parents suffered a damage rating of 7.7 in the CMS lines and 7.5 in the maintainer lines. For the yellow sugarcane aphid, M. sacchari, the CMS lines showed a damage rating of 4.0 compared to 3.2 for the maintainer lines (Fig. 1c). The resistant parents suffered a damage rating of 3.2 in the CMS lines and 2.0 in the maintainer lines, while the susceptible parents showed a damage rating of 5.0 in the CMS lines and 4.9 in the maintainer lines. Midge emergence was significantly lower in the panicles of midge-resistant maintainer lines than in the CMS lines (Fig. 1d). Midge emergence in panicles of midge-resistant CMS lines was very close to the panicles of midge-susceptible CMS or maintainer lines. Generally, CMS lines exhibited greater damage than their maintainer lines, suggesting that expression of resistance to sorghum midge may be influenced by the interaction of factors in the cytoplasm of maintainer lines with the nuclear genes.

Fig. 2. Insect damage in sorghum hybrids based on resistant (R) and susceptible (S) male-sterile and pollinator lines. a: Shoot fly, Atherigona soccata (FR1 = SPSFR 94006, FR2 = SPSFR 94007, FS1 = Tx 623A, and FS2 = CK 60A). b: Sorghum midge, Stenodiplosis sorghicola (MR1 = ICSA 88019, MR2 = ICSA 88020, MS1 = 296A, and MS2 = ICSA 42).

The shoot fly-resistant CMS lines showed 72.0% deadheart formation compared to 94.7% in the susceptible CMS lines (Fig. 2a). Hybrids based on resistant x resistant parents (SPSFR 94006A and SPSFR 94007A x resistant pollinator lines) showed 60.6 to 62.3% deadheart formation compared to 90.3 to 95.1% deadhearts in the hybrids based on susceptible x resistant and susceptible x susceptible parents (Tx 623A and CK 60A x resistant or susceptible pollinator lines). The resistant x susceptible hybrids (FR 1 x S and FR 2 x S) suffered 80.8 to 82.8% deadhearts.

The spikelets of midge-resistant maintainer lines (ICSB 88019 and ICSB 88020) suffered an average of 13.7% damage, while the midge-susceptible maintainer lines (296B and ICSB 42) suffered 40.5% midge damage (Fig. 2b). Sorghum midge damage in the resistant x resistant hybrids averaged 10.9%, while those based on resistant x susceptible parents suffered 22.2 to 24.6% damage. The susceptible x resistant hybrids suffered 32.5 to 32.6% midge damage, and susceptible x susceptible hybrids suffered 51.4 to 53.4% midge damage. Male-sterile lines showed a greater influence on the expression of resistance/susceptibility to shoot fly and sorghum midge than the pollinator lines.

Conclusion

Cytoplasmic nuclear male-sterility has been used for exploiting the heterotic potential for increasing crop production. Male-sterile lines are more susceptible to insects than their maintainer lines. Cytoplasmic nuclear male sterility in sorghum is due to the interaction between milo-cytoplasm and Kafir nuclear genes (Stephens and Holland 1954). For inducing sterility in Kafir cytoplasm, genes at both lociare required, whereas only onegene is required for inducing sterility in milo-cytoplasm. Insect-resistantCMS lines suffered more damage than the corresponding maintainer lines, and this may be due to factors associated with male-sterility or fertility restoration cytoplasm in sorghum (Sharma et al. 1994). Resistance to insects is largely governed by additive gene action, and resistance is needed in both parents to produce insect-resistant hybrids (Sharma et al. 1996). These findings have an important bearing for development and deployment of insect-resistant hybrids for sustainable crop production.

References

Kaul MLH (1988). Male sterility in higher plants. In Monographs.Theoretical and Applied Genetics (Frankel, R., Grossman, M. and Maliga, P., eds.). Volume 10. Springer, Berlin Heidelberg, New York.

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