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Review
. 2022 Jan 5:12:644424.
doi: 10.3389/fpls.2021.644424. eCollection 2021.

The Roles of Floral Organ Genes in Regulating Rosaceae Fruit Development

Jia-Long Yao  1 , Chunying Kang  2 , Chao Gu  3 , Andrew Peter Gleave  1
Affiliations
Review

The Roles of Floral Organ Genes in Regulating Rosaceae Fruit Development

Jia-Long Yao et al. Front Plant Sci. .

Abstract

The function of floral organ identity genes, APETALA1/2/3, PISTILLATA, AGAMOUS, and SEPALLATA1/2/3, in flower development is highly conserved across angiosperms. Emerging evidence shows that these genes also play important roles in the development of the fruit that originates from floral organs following pollination and fertilization. However, their roles in fruit development may vary significantly between species depending on the floral organ types contributing to the fruit tissues. Fruits of the Rosaceae family develop from different floral organ types depending on the species, for example, peach fruit flesh develops from carpellary tissues, whereas apple and strawberry fruit flesh develop from extra-carpellary tissues, the hypanthium and receptacle, respectively. In this review, we summarize recent advances in understanding floral organ gene function in Rosaceae fruit development and analyze the similarities and diversities within this family as well as between Rosaceae and the model plant species Arabidopsis and tomato. We conclude by suggesting future research opportunities using genomics resources to rapidly dissect gene function in this family of perennial plants.

Keywords: AP2; MADS-box; apple; fruit development; miR172; peach; strawberry.

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Conflict of interest statement

Authors AG and J-LY were employed by company The New Zealand Institute for Plant and Food Research Limited. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Phylogeny tree of floral MADS-box proteins and their gene expression in developing fruit tissues. (A) a Neighbor-Joining consensus tree was constructed using Geneious software (v10.0.9) with 1,000 bootstrap replicates after protein sequences were aligned using Geneious Alignment software (v10.0.9). MADS-box protein sequences downloaded from the reference genome of apple (Daccord et al., 2017), peach (Verde et al., 2013), strawberry (Edger et al., 2017), and Arabidopsis. The Arabidopsis protein IDs are AT1G69120.1 (AtAP1), AT5G60910.1 (AtFUL), AT5G20240.1(AtPI), AT3G54340.1 (AtAP3), AT4G18960.1 (AtAG), AT3G58780.1 (AtSHP1), AT2G42830.1 (AtSHP2), AT4G09960.1 (AtSTK), AT5G15800.1 (AtSEP1), AT3G02310.1 (AtSEP2), AT1G24260.1 (AtSEP3), AT2G03710.1 (AtSEP4), and AT5G10140.1 (AtFLC). (B) a heatmap shows the expression patterns of floral MADS-box genes in fruit tissues of peach and strawberry at five developmental stages (S1-S5) based on previously published RNA-seq data (Pei et al., 2020). Rosaceae Gene IDs are coded as: MD for apple (Malus domestica), Pp_XM for peach (based on Prunus_persica_NCBIv2) and FvH4 for strawberry (based on Frageria vesca H4). S1 to S5: 21, 42, 56, 84, and 105 days after full bloom for peach, and 11, 27, 31, 43, and 47 DAFB for strawberry.
Figure 2
Figure 2
Phylogeny tree of AP2-like proteins and their gene expression in developing fruit tissues. (A) a Neighbor-Joining consensus tree was constructed using Geneious software (v10.0.9) with 1,000 bootstrap replicates after protein sequences were aligned using Geneious Alignment software (v10.0.9). AP2-like protein sequences downloaded from the reference genome of apple, peach, strawberry, and Arabidopsis. The Arabidopsis protein IDs are AT4G36920.1 (AtAP2), AT2G28550.3 (AtTOE1), AT5G60120.2 (AtTOE1), AT5G67180.1 (AtTOE3), AT3G54990.1 (AtSMZ), AT2G39250.1 (AtSNZ), and AT4G37750.1 (AtANT). (B) a heatmap shows the expression patterns of AP2-like genes in fruit tissues of peach and strawberry at five developmental stages (S1-S5) based on previously published RNA-seq data (Pei et al., 2020). Rosaceae Gene IDs are coded as: MDs for apple (Malus domestica), Pp_XM for peach (based on Prunus_persica_NCBIv2), and FvH4 for strawberry (based on Frageria vesca H4). S1 to S5: 21, 42, 56, 84, and 105 days after full bloom for peach, and 11, 27, 31, 43, and 47 DAFB for strawberry. The arrows indicate AP2 genes predominantly expressed in fruits.
Figure 3
Figure 3
Apple flower and fruit phenotypes after alteration of the expression of floral organ genes. The images show open flowers (A–F) and mature fruit (G–L) of wild-type (A,G) and transgenic apple plants (B–F, H–L). miR172 is known to inhibit the expression of the AP2- and AP2-like genes. miR172 over-expression converts sepal segments to petal-like tissues (B) outer petals are removed to show sepal-petal conversion and dramatically reduces fruit size (H), wild-type fruit on left and transgenic fruit on right (Yao et al., 2015). Repressing expression of the MdPI gene converts petals to sepals, and stamens to carpels (C), and results in parthenocarpic (seedless) fruit with two whorls of carpels marked using two red arrows (I). However, over-expressing MdPI converts sepals to petals (p, petal; ep, ectopic petal) (D) and suppresses fruit tissue growth resulting in altered fruit shape (J) (Yao et al., 2001, 2018). Repressing expression of two AG homologs, MdMADS15/22, converts stamens to petals (E) and increases carpel number and therefore fruit locule number (K) (Klocko et al., 2016). Repressing expression of two SEP homologs, MdMADS8/9, partially converts petals to greenish sepal-like organs (F) and suppresses fruit flesh growth (L) (Ireland et al., 2013).
Figure 4
Figure 4
Flowers of apple transgenic plants over-expressing miR172. (A) Floral inflorescences show abnormal flowers consisting of leaf-like carpel tissues (lct), style, and stigma, but no sepals, petals, or stamens. (B) A florescence of (A) with leaf-like carpels removed reveals separate carpels consisting of ovary, style, and stigma. (C) A single carpel removed from the inflorescence in (B) reveals two ovules after cutting the ovary open (This figure is re-produced from Yao et al., 2015).
Figure 5
Figure 5
The apple floral organ genes regulate fruit development. The diagram shows the apple floral organ genes that have been functionally studied in apple transgenic plants. miR172 inhibits the expression of AP2-like genes that promote apple fruit flesh growth (Yao et al., 2015). Ectopic expression of MdPI inhibits fruit flesh growth (Yao et al., 2018) while knockout of MdPI promotes parthenocarpic fruit development (Yao et al., 2001). The AG/SHP homologs MADS14/15 are required for fruit core growth and coreless fruit can be produced by knocking out MADS14/15 (Schaffer et al., 2017; Ireland et al., 2021). The class E genes MdMADS8/9 are required for fruit flesh growth and fruit ripening (Ireland et al., 2013).
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