Gonzalez-Bayon, Rebeca; Shen, Yifei; Groszmann, Michael; Zhu, Anyu; Wang, Aihua; Allu, Annapurna D.; Dennis, Elizabeth; Peacock, W. James; Greaves, Ian K
Description
Hybrids are used extensively in agriculture due to their superior performance in seed yield and plant growth, yet the molecular mechanisms underpinning hybrid performance are not well understood. Recent evidence has suggested that a decrease in basal defense response gene expression regulated by reduced levels of salicylic acid (SA) may be important for vigor in certain hybrid combinations. Decreasing levels of SA in the Arabidopsis (Arabidopsis thaliana) accession C24 through the introduction...[Show more] of the SA catabolic enzyme salicylate1 hydroxylase (NahG) increases plant size, phenocopying the large-sized C24/Landsberg erecta (Ler) F1 hybrids. C24♀ × Ler♂ F1 hybrids and C24 NahG lines shared differentially expressed genes and pathways associated with plant defense and leaf senescence including decreased expression of SA biosynthetic genes and SA response genes. The expression of TL1 BINDING TRANSCRIPTION FACTOR1, a key regulator in resource allocation between growth and defense, was decreased in both the F1 hybrid and the C24 NahG lines, which may promote growth. Both C24 NahG lines and the F1 hybrids showed decreased expression of the key senescence-associated transcription factors WRKY53, NAC-CONTAINING PROTEIN29, and ORESARA1 with a delayed onset of senescence compared to C24 plants. The delay in senescence resulted in an extension of the photosynthetic period in the leaves of F1 hybrids compared to the parental lines, potentially allowing each leaf to contribute more resources toward growth.
Hybrid vigor describes the superior performance of hybrid crop plants relative to their parents in important agronomic traits such as biomass and seed yield (reviewed by Chen, 2013). Hybrids in maize (Zea mays), rice (Oryza sativa), and canola (Brassica napus) have increased seed yield and are used extensively in agriculture. Hybrid vigor is associated with alterations in gene expression profiles resulting from interactions between the two parental genomes present in the one nucleus. Changes in patterns of gene activity due to dominance, overdominance, and epistasis have been proposed to explain the hybrid vigor phenotype (reviewed by Fu et al., 2015); how this is achieved on a genomic level is not understood.
In Arabidopsis (Arabidopsis thaliana), F1 hybrids develop at a faster rate than parental lines, resulting in an increase in biomass and seed yield (Groszmann et al., 2014; Zhu et al., 2016; Wang et al., 2017). The increase in growth rate can occur at different stages of plant development and differs among hybrid lines (Groszmann et al., 2014). In C24/Col hybrid seedlings, the increased growth rate was observed at 3–4 d after sowing (DAS; Meyer et al., 2012). The differences in enhanced growth during different developmental stages highlight the importance of defining stages of development critical for the observed phenotypic vigor. The increase in hybrid biomass may result from altered patterns of expression in circadian rhythm genes affecting photosynthetic and other metabolic genes essential for growth (Ni et al., 2009; Shen et al., 2012; Groszmann et al., 2014; Miller et al., 2015; Wang et al., 2017). Some hybrids have increased expression levels of genes involved in the biosynthesis, signaling, and transport of auxin, a hormone that promotes plant growth through the regulation of cell proliferation and cell expansion (Perrot-Rechenmann, 2010; Shen et al., 2012; Wang et al., 2017). In F1 hybrids, the changes in auxin biosynthesis and signaling may result from increased levels of PHYTOCHROME INTERACTING FACTOR4 (PIF4), which regulates genes in the auxin biosynthesis and signaling pathways (Wang et al., 2017).
Some hybrid systems show a decrease in basal expression of defense response genes in the seedling, which, in the absence of pathogens, may increase resource allocation to plant growth, potentially contributing to hybrid vigor (Groszmann et al., 2015; Miller et al., 2015; Yang et al., 2017). Conversely, altering the growth-defense balance toward defense can result in hybrid weakness, where hybrids with hyperactivated defense pathways have reduced growth (Todesco et al., 2010). Hybrids with a decrease in basal defense gene expression may have an associated decrease in the level of salicylic acid (SA; Groszmann et al., 2015). Reduced levels of SA in the Arabidopsis accession C24 using the bacterial degradative enzyme salicylate1 hydroxylase (NahG), phenocopies hybrid vigor including the increased plant size, suggesting that SA-regulated pathways may have an important role in certain hybrid combinations (Groszmann et al., 2015).
We determined whether the size increases of F1 hybrids and C24 NahG lines result from changes to the expression level of genes in the same pathways. In both genotypes the decrease in SA is associated with reduced expression of basal defense response genes and a delay in senescence, both of which may promote increased growth.
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