Senescence and Defense Pathways Contribute to Heterosis

Abstract

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 of the SA catabolic enzyme salicylate1 hydroxylase (NahG) increases plant size, phenocopying the large-sized C24/Landsberg erecta (Ler) F1 hybrids. C24♀ 3 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.

In Arabidopsis hybrids and Hybrid Mimics, up‐regulation of cell wall biogenesis is associated with the increased plant size

“…Some genes in the defense response pathway are also involved in the leaf senescence pathway (Gonzalez‐Bayon et al, ). Senescence genes had decreased expression in the Ws/L er Hybrid Mimics and increased transcript levels in one Ws/L er small line.…”

“…In C24/L er F1 hybrids, changes in defense and stress response gene expression are consistent with a reduction in transcription of basal defense genes (Groszmann et al, ; Miller et al, ). The decreased expression of defense response genes may contribute to the increased growth of the hybrids compared with the average growth of parents through changes in expression of the regulator ARABIDOPSIS THALIANA CLASS B HEAT SHOCK FACTOR B1 (TBF1) (Gonzalez‐Bayon et al, ; Pajerowska‐Mukhtar et al, ), which is involved in the control of the balance between growth and defense. C24 has high levels of salicylic acid (SA) which do not affect its growth but hybrids with C24 as one parent have a decreased level of SA relative to C24 and down‐regulated defense pathway genes (Bechtold et al, ; Groszmann et al, ).…”

“…Down-regulation of defense response genes has been reported to result in the up-regulation of growth genes and contribute to heterosis in hybrids having C24 as one parent (Gonzalez-Bayon et al, 2019;Groszmann et al, 2015;Miller, Song, Shi, Juenger, & Chen, 2015;Wang et al, 2015). In the rosette leaves of 25-day-old Ws/Ler hybrids, 49 DEGs were associated with "defense response"; the majority (35 genes) were down-regulated in the F1 hybrids and Mimics (Table S10).…”

“…Some genes in the defense response pathway are also involved in the leaf senescence pathway (Gonzalez-Bayon et al, 2019).…”

Salicylic Acid, Senescence, and Heterosis

“…In this issue of Plant Physiology, Ian Greaves' group at CSIRO Agriculture and Food in Canberra further explored the basis of heterosis in C24 3 Ler hybrids of Arabidopsis (Gonzalez-Bayon et al, 2019). This study builds on their previous body of work showing that hormone pathway and biotic response genes are differently expressed in hybrids of C24 3 Ler, C24 3 Col-0, and Col-0 3 Ler (Groszmann et al, 2015).…”