The flowers and fruits of male, female, and hermaphrodite papaya. (A) Female flowers; (B) hermaphrodite flowers; (C) male flowers; (D) female fruit; (E) hermaphrodite fruit; (F) male tree. 

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Context 1

... ( Carica papaya ) belongs to the small family Caricaceae with six genera and 35 species, of which 32 are dioecious, two trioecious, and one monoecious. Papaya is a fast growing, rarely branching, semi-woody tropical fruit tree with a short juvenile phase of 3 to 8 months. Once it starts flowering, it will continue to flower and produce fruit throughout the year. Papaya is cultivated in tropical and subtropical regions world- wide. Papaya fruit is the most nutritious of the 35 commonly consumed fruits based on percentage of US recommended daily allowance for vitamins A and C, folate, potassium, niacin, thi- amin, iron, riboflavin, calcium, and fiber [1–3]. Papaya is also cultivated for its milky latex that contains the proteolytic enzyme papain used for hydrolyzing beer peptides (chillproofing), ten- derizing meats, and medicinal applications. Papaya is diploid with 9 pairs of chromosomes. It has a small genome of 372 Mb [4] and a generation time as short as 9 months. Vegetative propagation is possible by inducing root- ing from cuttings or by micro-propagating in tissue culture. A genetic transformation system is well established. Transgenic papaya varieties conferring resistance to papaya ringspot virus saved the Hawaii papaya industry from collapse in the mid-1990s [5]. The above favorable properties make papaya an excellent model system for genomic research. Moreover, papaya is in the order Brassicales that includes the well-studied Brassica and Arabidopsis. Both are in the family Brassicaceae that diverged from a common ancestor with Caricaceae about 72 million years ago (MYA) [6] and can thus serve as an outgroup for comparative and phylogenetic analyses of Brassicaceae genomes. Papaya is somewhat unusual in that it is trioecious with three basic sex forms: female, male, and hermaphrodite. Cymose inflorescences arise in axils of leaves. The type of inflores- cence produced depends on the sex of the tree (Fig. 1). Varieties typically are either dioecious (with unisexual flowers and exclu- sively male and female plants) or gynodioecious (with bisexual and unisexual flowers and hermaphrodite and female plants). Male trees are characterized by long, pendulous, many-flowered inflorescences bearing slender male flowers lacking a pistil, except for occasional pistil-bearing flowers at the distal termi- nus. Female trees have short inflorescences with few flowers bearing large functional pistils without stamens. Hermaphroditic trees have short inflorescences bearing bisexual flowers that can be sexually variable. Not only are the sex forms morphologically distinct, they are inherited in unexpected ratios that are due to a lethal factor associated with male dominant alleles (Table 1). Hermaphrodite papaya trees are primarily self-pollinated. However, seeds from selfed hermaphrodite trees always segregate into hermaphrodites and females at the ratio 2:1. Seeds from female trees segregate at the hermaphrodite to female ratio of 1:1 if they were fertilized by pollen from a hermaphrodite tree, or a ratio of 1:1 male to female when fertilized by pollen from a male tree. Male trees are never produced when hermaphrodites are selfed or when hermaphrodites are used as a pollen source to fertilize female trees. However, male trees occur at a ratio of 2 male:1 female when the occasional male fruit is selfed, or 1 male:1 hermaphrodite: 1 female when male pollen fertilizes the pistil of hermaphrodite trees. These unexpected sex form ratios have been the subject of extensive studies. In many regions of the world, hermaphrodites are preferred for their higher productivity since every tree will produce fruit, whereas using female trees for fruit production involves the loss of 6–10% of field space for growing male trees to pol- linate the females. However, in subtropical regions with cool winters, female production is preferred because female flowers are stable at low temperature while hermaphrodite flowers tend to fuse anthers to the carpels and produce deformed carpellodic fruit. The lack of true breeding hermaphrodite varieties results in reduced productivity due to sex segregation in seedlings and has been a problem since the beginning of papaya cultivation that persists to this day [7]. Farmers using hermaphrodites for production need to germinate a minimum of five seedlings per hill to assure there are no more than 3% female trees. The five plants in a hill must be grown for 4–6 months until sexes can be deter- mined. Finally, roguing must be practiced to obtain sex ratios conducive to optimal productivity. This process is inefficient of time, labor, water, and nutrients, and also results in delayed production due to competition among the plants in early growth. On the other hand, farmers depending on female tree production need to germinate four seedlings per hill to keep 6 to 10% male trees in the field. The sex determination system in papaya is particularly intriguing, not only because it has three sex types within the species, but also because it shows frequent sex reversal caused by environmental factors [8,9]. Recent advancements in genomics and molecular biology have provided tools and resources to allow us to characterize the sex determination system in papaya. In this paper we will review the past hypotheses of sex determination in papaya and our current understanding of the sex determination mechanisms learned from recent genomic and molecular evidence. Sex determination of papaya has attracted the attention of generations of geneticists and breeders because of its intriguing biology and the economic problems caused by segregation of sex types in papaya production. Before the application of molecular techniques in papaya research, there was little evidence to prove or disprove various hypotheses proposed over the years. Never- theless, some of the hypotheses provided partial revelations into the nature of sex determination in papaya. Based on the segregation ratios from crosses among three sex types (Table 1), Hofmeyr and Storey independently proposed that sex determination in papaya is controlled by a single gene with three alleles, named as M 1 , M 2 , and m by Hofmeyr and M , M h , and m by Storey [8,10,11]. We will follow Storey’s designa- tion for its convenience to separate the hermaphrodite allele M h from male allele M . Male individuals ( Mm ) and hermaphrodite individuals ( M h m ) are heterozygous, whereas female individuals ( mm ) are homozygous recessive. The dominant combinations of MM , M h M h , and MM h are lethal, resulting in a 2:1 segregation of hermaphrodite to female from self-pollinated hermaphrodite seeds and a 1:1 segregation of male to female or hermaphrodite to female from cross-pollinated female seeds. One year after Hofmeyr proposed the one-gene-with-three- allele hypothesis, he published an alternative genic balance hypothesis for sex determination in papaya [9,12]. Although there was no evidence of heteromorphic sex chromosomes, Hofmeyr suggested that the chromosomes bearing the M , M h , and m alleles were “sex chromosomes.” In this hypothesis, it is assumed that female sex determining factors predominate the “sex chromosomes” while the male sex determining factors are in the autosome. It was further assumed that M and M h represent an inactivated region of the sex chromosomes where vital genes were eliminated, but that the inactivated region represented by M is longer than that represented by M h . The different sex types were the results of genic balance between the sex chromosomes and autosome. Because vital genes were missing in the inactivated regions of M and M h , any combinations of MM , MM h , M h M h would be lethal, while Mm and M h m would be viable because an m sex chromosome is present in each genotype. Hofmeyr went further to assign arbitrary numbers to each sex chromosome and the autosome to come up with a quantitative representation of the genic balance. Although his experiments on induced polyploidy in papaya tended to support the hypothesis, they were not conclusive [13]. Storey [14] revised his hypothesis about a single gene with three alleles to one involving a group of closely linked genes that are confined to a small region on the sex chromosome within which recombination is suppressed. Storey’s modified hypothesis is mainly based on the observation that long peduncles are always associated with male flowers but not with hermaphrodite or female flowers and that the lethal factor is associated only with male and hermaphrodite homozygous dominant genotypes. Genes located in the sex determination segment were postulated to ...

Context 2

... is somewhat unusual in that it is trioecious with three basic sex forms: female, male, and hermaphrodite. Cymose inflorescences arise in axils of leaves. The type of inflores- cence produced depends on the sex of the tree (Fig. 1). Varieties typically are either dioecious (with unisexual flowers and exclu- sively male and female plants) or gynodioecious (with bisexual and unisexual flowers and hermaphrodite and female plants). Male trees are characterized by long, pendulous, many-flowered inflorescences bearing slender male flowers lacking a pistil, except for ...