Regulatory change at Physalis Organ Size 1 correlates to natural variation in tomatillo reproductive organ size

Abstract

The genetic basis of size variation in the reproductive organs of tomatillo (Physalis philadelphica) is unknown. Here we report that the expression levels of the gene Physalis Organ Size 1 (POS1) are positively associated with size variation in P. philadelphica reproductive organs such flowers, berries and seeds. POS1 knockdown results in smaller flowers and berries with smaller cells as compared with their wild-type counterparts. Conversely, POS1 overexpression promotes organ size without increasing the cell number. The first introns of the POS1 alleles from the large, intermediate and small tomatillo groups contain one, two and three 37-bp repeats, respectively. Furthermore, our results show that copy variation of repeats in the first intron of POS1 alleles results in differential expression of this gene. Thus, co-variation in tomatillo reproductive organ sizes can be attributed to the novel regulatory variation in POS1.

Parallel vs. Convergent Evolution in Domestication and Diversification of Crops in the Americas

“…In tomato and Mexican green tomato (P. philadelphica), development of large fruits in domesticated accessions of both species initially seems to be an example of parallel phenotypic evolution in species belonging to the same family. But on closer examination, large fruits in tomato are found to result from increased numbers of cells in various parts of the fruit, together with more carpels in the fruit, while in Mexican green tomato, large fruits are due primarily to increased cell size (Wang et al, 2014). Carpel number, cell size and cell number are controlled by different genes so, not surprisingly, large fruits in tomato and Mexican green tomato are controlled principally by non-homologous genes.…”

“…An initial phase of cell division in a developing organ is usually followed by a phase of cell expansion. In the Mexican green tomato (Physalis philadelphica), Wang et al (2014) identified a locus that they named PHYSALIS ORGAN SIZE 1 (POS1). Overexpression of this locus resulted in larger organs, including fruits, whereas virus-induced silencing reduced sizes of these organs.…”

The Evolution of Diverse Floral Morphologies

“…A recent study in tomatillo (Physalis phyladelphica) exploited natural variation in size of floral organs to identify a new regulator of cell expansion, Physalis Organ Size 1 (POS1). POS1 encodes a new type of AP2-domain protein that promotes cell expansion and thus larger size in all floral organs [46]. Interestingly, POS1 homologs are only found in the Solanaceae, highlighting the importance of studying the mechanisms controlling organ size in non-model organisms to understand how evolution generates morphological diversity.…”

Bridging evolution and development in plants

“…Hongzhi Kong (Institute of Botany, Chinese Academy of Sciences, Beijing, China) reported that differences in floral meristem sizes and the flexibility in the expression of floral organ identity genes have contributed to the great variation in floral organ numbers in the spirally patterned Nigella damascena (Ranunculaceae) (Wang et al ., ). In fruits, Chaoying He (Institute of Botany, Chinese Academy of Sciences, Beijing, China) showed that the heterotopic expression of MADS‐BOX GENE 2 FROM PHYSALIS FLORIDANA ( MPF2 ) contributes to the formation of the Chinese lantern (a papery calyx) while heterochronic changes in PHYSALIS ORGAN SIZE 1 ( POS1) and POS2 expression are correlated with the variation of berry size among species in Physalis (Solanaceae) (He & Saedler, ; Wang et al ., ).…”