Hybrid Incompatibility of the Plant Immune System: An Opposite Force to Heterosis Equilibrating Hybrid Performances

Hybridization is a core element in modern rice breeding as beneficial combinations of two parental genomes often result in the expression of heterosis. On the contrary, genetic incompatibility between parents can manifest as hybrid necrosis, which leads to tissue necrosis accompanied by compromised growth and/or reduced reproductive success. Genetic and molecular studies of hybrid necrosis in numerous plant species revealed that such self-destructing symptoms in most cases are attributed to autoimmunity: plant immune responses are inadvertently activated in the absence of pathogenic invasion. Autoimmunity in hybrids predominantly occurs due to a conflict involving a member of the major plant immune receptor family, the nucleotide-binding domain and leucine-rich repeat containing protein (NLR; formerly known as NBS-LRR). NLR genes are associated with disease resistance traits, and recent population datasets reveal tremendous diversity in this class of immune receptors. Cases of hybrid necrosis involving highly polymorphic NLRs as major causes suggest that diversified R gene repertoires found in different lineages would require a compatible immune match for hybridization, which is a prerequisite to ensure increased fitness in the resulting hybrids. In this review, we overview recent genetic and molecular findings on hybrid necrosis in multiple plant species to provide an insight on how the trade-off between growth and immunity is equilibrated to affect hybrid performances. We also revisit the cases of hybrid weakness in which immune system components are found or implicated to play a causative role. Based on our understanding on the trade-off, we propose that the immune system incompatibility in plants might play an opposite force to restrict the expression of heterosis in hybrids. The antagonism is illustrated under the plant fitness equilibrium, in which the two extremes lead to either hybrid necrosis or heterosis. Practical proposition from the equilibrium model is that breeding efforts for combining enhanced disease resistance and high yield shall be achieved by balancing the two forces. Reverse breeding toward utilizing genomic data centered on immune components is proposed as a strategy to generate elite hybrids with balanced immunity and growth.