| Summary: | Betalains are water-soluble nitrogen-containing pigments with multiple bioactivities. Pitayas are the only at large-scale commercially grown fruit containing abundant betalains for consumers. Currently, the key genes involved in betalain biosynthesis remain to be fully elucidated. Moreover, genome-wide analyses of these genes in betalain biosynthesis are not available in betalain-producing plant species. In this study, totally 53 genes related to betalain biosynthesis were identified from the genome data of <i>Hylocereus undatus</i>. Four candidate genes i.e., one cytochrome P-450 R gene (<i>HmoCYP76AD1</i>), two L-DOPA 4,5-dioxygenase genes (<i>HmoDODAα1</i> and <i>HmoDODAα2</i>), and one cyclo-DOPA 5-O glucosyltransferase gene (<i>HmocDOPA5GT</i>) were initially screened according to bioinformatics and qRT-PCR analyses. Silencing <i>HmoCYP76AD1</i>, <i>HmoDODA</i><i>α1</i>, <i>HmoDODA</i><i>α2</i> or <i>HmocDOPA5GT</i> resulted in loss of red pigment. <i>HmoDODA</i><i>α1</i> displayed a high level of L-DOPA 4,5-dioxygenase activity to produce betalamic acid and formed yellow betaxanthin. Co-expression of <i>HmoCYP76AD1</i>, <i>HmoDODAα1</i> and <i>HmocDOPA5GT</i> in <i>Nicotiana benthamiana</i> and yeast resulted in high abundance of betalain pigments with a red color. These results suggested that <i>HmoCYP76AD1</i>, <i>HmoDODAα1</i>, and <i>HmocDOPA5GT</i> play key roles in betalain biosynthesis in <i>Hylocereus</i>. The results of the present study provide novel genes for molecular breeding programs of pitaya.
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