Early changes of gene activity in developing seedlings of Arabidopsis hybrids relative to parents may contribute to hybrid vigour

Zhu, Anyu; Greaves, Ian K.; Liu, Pei-Chuan; Wu, Limin; Dennis, Elizabeth S.; Peacock, W. James

doi:10.1111/tpj.13285

Cited by 42 publications

(42 citation statements)

References 33 publications

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“…The C24/ Ler F1 hybrids germinate earlier than the parents (7). In the present experiment, both reciprocal hybrids and the three hybrid mimic lines had germination times ∼10-12 h ahead of the parents [34 vs.…”

Section: Significancementioning

confidence: 57%

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PIF4-controlled auxin pathway contributes to hybrid vigor in Arabidopsis thaliana

Wang

Greaves

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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F1 hybrids in Arabidopsis and crop species are uniform and high yielding. The F2 generation loses much of the yield advantage and the plants have heterogeneous phenotypes. We generated pure breeding hybrid mimic lines by recurrent selection and also selected a pure breeding small phenotype line. The hybrid mimics are almost completely homozygous with chromosome segments from each parent. Four particular chromosomal segments from C24 and 8 from Ler were present in all of the hybrid mimic lines, whereas in the F6 small phenotype line, the 12 segments were each derived from the alternative parent. Loci critical for promoting hybrid vigor may be contained in each of these 12 conserved segments. We have identified genes with similar altered expression in hybrid mimics and F1 plants but not in the small phenotype line. These genes may be critical for the generation of hybrid vigor. Analysis of transcriptomes indicated that increased expression of the transcription factor PHYTOCHROME-INTERACTING FACTOR (PIF4) may contribute to hybrid vigor by targeting the auxin biosynthesis gene YUCCA8 and the auxin signaling gene IAA29. A number of auxin responsive genes promoting leaf growth were up-regulated in the F1 hybrids and hybrid mimics, suggesting that increased auxin biosynthesis and signaling contribute to the hybrid phenotype. The hybrid mimic seeds had earlier germination as did the seeds of the F1 hybrids, indicating cosegregation of the genes for rosette size and the germination trait. Early germination may be an indicator of vigorous hybrids.heterosis | transcription factor | biomass | transregulation | germination T wo features common to hybrids in many crops are the increased yield and phenotypic uniformity of the F1 hybrid generation and the reduced yield and phenotypic heterogeneity of the F2 generation (1). These characteristics also apply to the F1 and F2 populations in Arabidopsis hybrids (2). The processes of capture of light and assimilation of CO 2 into photosynthate are the same in the hybrid and parents and as the hybrids have larger leaves than their parents, they produce more photosynthate (3).In a previous paper (2), transcriptome analyses showed that in the hybrids, most genes are expressed at the same levels as in the parents. Compared with the average level of gene expression in the parents, ∼2,000 genes (6% of the genome) have altered expression in the hybrids and are likely to be involved in the generation of the hybrid vigor phenotype. Many of the differentially expressed genes (DEGs) encode proteins in key metabolic pathways such as the plant hormone systems auxin and salicylic acid (SA) and the basal defense response, suggesting that these pathways contribute to the development of hybrid vigor (4). Altered hormone abscisic acid (ABA) and defense response have also been reported in rice hybrids (5). Despite the contrasting phenotypes of the F1 and F2 populations, we were able to develop "pure breeding" F5/F6 lines with phenotypes comparable to the F1 hybrids (hybrid mimics) (2). The hybrid mimic...

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Section: Significancementioning

confidence: 57%

“…The C24/Ler F1 hybrids showed growth vigor relative to parents as early as the first week after sowing (7). Heterosis was well established at 7 DAS in both reciprocal hybrids with cotyledon areas exceeding the MPV by 6.5% and 22.7% (7).…”

Section: Significancementioning

confidence: 94%

PIF4-controlled auxin pathway contributes to hybrid vigor in Arabidopsis thaliana

Wang

Greaves

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…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).…”

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confidence: 99%

Senescence and Defense Pathways Contribute to Heterosis

et al. 2019

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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.

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“…Hybrids and Hybrid Mimic lines showed similarity in growth patterns as measured by increased rosette diameter compared with MPV (Figure a,b and Figure a,b). As in the C24/L er hybrids (Zhu et al, ), both Ws/L er and Col/L er hybrids germinated earlier than the parent lines (Table ). At 28 hr after sowing (HAS), 90% of Col/L er hybrid seeds had germinated, approximately 3 hr ahead of the seeds of parental lines.…”

Section: Resultsmentioning

confidence: 50%

“…The expression data for each gene were normalized to the expression of the housekeeping gene At4g26410 (Czechowski, Stitt, Altmann, Udvardi, & Scheible, 2005). The following primers were used: As in the C24/Ler hybrids (Zhu et al, 2016), both Ws/Ler and Col/ Ler hybrids germinated earlier than the parent lines (Table 1) Table S1).…”

Section: Real-time Pcrmentioning

confidence: 99%

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

Wang

Greaves

et al. 2019

Plant Direct

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Hybrid breeding is of economic importance in agriculture for increasing yield, yet the basis of heterosis is not well understood. In Arabidopsis, crosses between different accessions produce hybrids with different levels of heterosis relative to parental phenotypes in biomass. In all hybrids, the advantage of the F1 hybrid in both phenotypic uniformity and yield gain is lost in the heterogeneous F2. F5/F6 Hybrid Mimics generated from a cross between C24 and Landsberg erecta (Ler) ecotypes demonstrated that the large plant phenotype of the F1 hybrids can be stabilized. Hybrid Mimic selection was applied to Wassilewskija (Ws)/Ler and Col/Ler hybrids. The two hybrids show different levels of heterosis. The Col/Ler hybrid generated F7 Hybrid Mimics with rosette diameter and fresh weight equivalent to the F1 hybrid at 30 DAS; F7 Ws/Ler Hybrid Mimics outperformed the F1 hybrid in both the rosette size and biomass. Transcriptome analysis revealed up‐regulation of cell wall biosynthesis, and cell wall expansion genes could be a common pathway in increased size in the Arabidopsis hybrids and Hybrid Mimics. Intercross of two independent Hybrid Mimic lines can further increase the biomass gain. Our results encourage the use of Hybrid Mimics for breeding and for investigating the molecular basis of heterosis.

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Early changes of gene activity in developing seedlings of Arabidopsis hybrids relative to parents may contribute to hybrid vigour

Cited by 42 publications

References 33 publications

PIF4-controlled auxin pathway contributes to hybrid vigor in Arabidopsis thaliana

PIF4-controlled auxin pathway contributes to hybrid vigor in Arabidopsis thaliana

Senescence and Defense Pathways Contribute to Heterosis

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

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