Genetic regulation of maize flower development and sex determination

Planta, Oct 2016

Main conclusion The determining process of pistil fate are central to maize sex determination, mainly regulated by a genetic network in which the sex-determining genes SILKLESS 1 , TASSEL SEED 1 , TASSEL SEED 2 and the paramutagenic locus Required to maintain repression 6 play pivotal roles. Maize silks, which emerge from the ear shoot and derived from the pistil, are the functional stigmas of female flowers and play a pivotal role in pollination. Previous studies on sex-related mutants have revealed that sex-determining genes and phytohormones play an important role in the regulation of flower organogenesis. The processes determining pistil fate are central to flower development, where a silk identified gene SILKLESS 1 (SK1) is required to protect pistil primordia from a cell death signal produced by two commonly known genes, TASSEL SEED 1 (TS1) and TASSEL SEED 2 (TS2). In this review, maize flower developmental process is presented together with a focus on important sex-determining mutants and hormonal signaling affecting pistil development. The role of sex-determining genes, microRNAs, phytohormones, and the paramutagenic locus Required to maintain repression 6 (Rmr6), in forming a regulatory network that determines pistil fate, is discussed. Cloning SK1 and clarifying its function were crucial in understanding the regulation network of sex determination. The signaling mechanisms of phytohormones in sex determination are also an important research focus.

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Genetic regulation of maize flower development and sex determination

Planta Genetic regulation of maize flower development and sex determination Qinglin Li 0 1 2 Baoshen Liu 0 1 2 0 College of Agronomy/State Key Laboratory of Crop Biology, Shandong Agricultural University , Daizong Road No. 61, Taian 271018, Shandong , China 1 & Baoshen Liu 2 & Qinglin Li Main conclusion The determining process of pistil fate are central to maize sex determination, mainly regulated by a genetic network in which the sex-determining genes SILKLESS 1, TASSEL SEED 1, TASSEL SEED 2 and the paramutagenic locus Required to maintain repression 6 play pivotal roles. Maize; Flower development; Sex determination; Gene and phytohormone function; Regulatory network - pistil fate, is discussed. Cloning SK1 and clarifying its function were crucial in understanding the regulation network of sex determination. The signaling mechanisms of phytohormones in sex determination are also an important research focus. Introduction Maize (Zea mays L.) is monoecious with two types of unisexual inflorescences located on different parts of the plant, the male tassel and the female ear. Many sex-determining mutants have been identified, contributing to this species becoming a model to study the molecular mechanisms of flower development in grasses (Hua 1998; Yang and Li 2012) . Maize ear bears only pistillate florets, from which elongated functional stigmas, known as silks, emerge. If silk development is abnormal, pollination is affected, and seed production and yield are significantly reduced. Researches on maize sex mutants started early and began with the study of a mutant silkless (sk1) (Jones 1925) . Previous studies indicated that sex-determining genes such as silk identity gene SILKLESS 1 (SK1), in combination with phytohormones, play important roles in maize sex determination (Cheng et al. 1983; Veit et al. 1993; Dellaporta and Calderon-Urrea 1994; Young et al. 2004; Chuck 2010) . In this review, we give a detailed introduction of maize flower development process (Fig. 1) and discuss the regulation of maize sex determination. Most flowers, especially some eudicot flowers typically have four floral organs that arise in concentric rings called whorl. These whorls are numbered in ascending order from outside to inside, and comprise sepals, petals, stamens, and carpels (Krizek and Fletcher 2005). One carpel may produce one or more ovules and at least one stigma on the top of each ovule (Theißen et al. 2000; Krizek and Fletcher 2005) . At a rudimentary level, maize has a similar floral structure to eudicots, and maize carpel is also referred to as pistil (Fig. 2b). Spikelet are the basic unit of maize inflorescence, on the outer edge of which, a pair of glumes (outer glume and inner glume) encloses two immature florets, the primary floret (upper floret, UF) and the secondary floret (lower floret, LF) (Cheng et al. 1983; Le Roux and Kellogg 1999) . All immature florets are initially bisexual, and consist of a single, central pistil polymerized from three carpels and three stamens surrounded by two lodicules, a palea, and a lemma (Dellaporta and Calderon-Urrea 1994; Irish 1996) (Fig. 1c). In mature tassel spikelet, all upper floret and lower floret are unisexual male florets with only three stamens and surrounded by two lodicules, a palea and a lemma but no pistil (Cheng et al. 1983; Dellaporta and Calderon-Urrea 1994; Irish 1996) (Fig. 1e). In mature ear prior to sex differentiation. d Structure diagram of spikelet underway sex differentiation. e Structure diagram of mature spikelet at unisexual stage Fig. 2 The ‘ABCDE model’ of floral organ identity and flower c structure in Arabidopsis and maize (modified from Theißen 2001; Theißen and Saedler 2001; Whipple et al. 2004; Bommert et al. 2005a, b; Krizek and Fletcher 2005; Thompson and Hake 2009) . In Arabidopsis, sepals, petals, stamens, carpels, and ovules are specified by A, A and B, B and C, C, D homeotic functions, respectively. E functions contribute to four whorl floral organs’ identity. In maize, A, A and B, B and C, C function, respectively, in specifying identity of paleas and lemmas, lodicules, stamens, and carpels identity. D functions mainly in specifying ovule identity and E genes are required for all floral organ development. b Flower structure and organs of Arabidopsis and maize, the ‘quartet model’ of floral organ specification in Arabidopsis. In maize bisexual flower, palea and lemma are homologous to sepals of Arabidopsis, lodicules are homologous to petals; glumes are considered as the bract-like structures and there is not reliable evidence to verify glumes share homology with Arabidopsis floral organ. Based on the ‘quartet model’, floral MADS protein complexes are assumed to form when they specifically bind to CArG [CC(A/T6GG)] box binding sites in the promoters of target genes, and they regulate the transcription of floral organs’ identity genes. In Arabidopsis, the predicted compositions of protein complexes in the four whorls are: AP1-AP1-SEP-SEP in whorl 1; AP1-SEP-AP3-PI in whorl 2; AP3-PI-SEP-AG in whorl 3; AG-AGSEP-SEP in whorl 4 (a). Here, we suggest a hypothesis composition STK-SEP-SHP-SHP to specify ovules in whorl 4 (b). The antagonism between the A and C genes may be caused by the reciprocal inhibition of the complexes that contain AP1 and AG proteins, and that complexes containing AP1 repress TERMINAL FLOWER 1 (TFL1) expression. Blue imaginary lines genes or proteins with floral homeotic functions; barred lines antagonistic interactions; hyphen heterodimer formation; comma unknown interaction; yellow barred lines SK1 functions are presumptions; blue ‘?’ activation or potentiation for the formation of floral organ identity; ‘?’ the part is still unknown; and yellow imaginary lines the scheme is an assumption spikelet, there are one ovule with a single silk on the top, two lodicules, and a palea and a lemma on the outer edge in upper floret (Cheng et al. 1983) (Fig. 1e). Developmental process of maize floral organ In maize flower development process, the inflorescence meristems (IMs) of tassel and ear, respectively, develop from shoot apical meristems (SAMs) and axillary meristems (AMs) (Tanaka et al. 2013) . During tassel development, IMs initiate branch meristems (BMs) first, and then IMs and BMs successively initiate spikelet pair meristems (SPMs), which give rise to two spikelet meristems (SMs) (Fig. 1a). SMs form a pair of glumes, after which upper floret meristems (UFMs) and lower floret meristems (LFMs) are successively initiated and develop into upper florets and lower florets, respectively (Chuck et al. 2002; Thompson et al. 2009) (Fig. 1a). The inflorescence development of ear is similar to tassel inflorescence development, with the exception that no BMs are formed (Krizek and Fletcher 2005) (Fig. 1a). During floret development, upper floret meristem develops slightly earlier than lower floret meristem, and the lemmas of upper floret and lower floret (inner and outer lemma) are formed first. Then upper floret meristem initiates three stamen primordia, followed by a pistil composed of three carpel primordia. Then palea emerges in the gap between upper floret and lower floret, with two lodicules surrounding three developing stamens (Cheng et al. 1983) . In the following development process, all florets undergo selective development, in which programmed cell death (PCD) signals play important roles in sex differentiation (Calderon-Urrea and Dellaporta 1999; Yamasaki et al. 2005; Bortiri and Hake 2007; Kim et al. 2007) . Then, in tassel spikelet, the stamen primordia of florets preferentially develop and eventually covert into anthers, the pistil of upper floret and lower floret successively abort after initiation (Cheng et al. 1983). In ear spikelet, the pistil primordia of upper floret initiates fast and develops successfully, then the stamens of upper floret and the pistil of lower floret gradually abort, and later the pistil of upper floret produces an ovule with a silk, three stamens of lower floret degenerate with the abortion of lower floret at the last (Cheng et al. 1983) (Fig. 1c–e). Thus, tassel florets develop into unisexual male florets and upper florets of ear develop into unisexual female florets upon maturation (Cheng et al. 1983; Thompson et al. 2009; Tanaka et al. 2013) . Floral organ identity MADS-box genes, small RNAs, micro RNAs, and even daedal networks, consisting of MADS-box genes and phytohormones, play important roles in the regulation of floral organ development (Hollick et al. 2005; Parkinson et al. 2007; Banks 2008; Gallavotti et al. 2010; Tanaka et al. 2013; Liu et al. 2014) . In the classic ‘ABC model’ of flower development proposed for Arabidopsis, three functional classes of MADS-box genes (A, B, and C) work independently or in combination to determine the identity of four whorl floral organs (Coen and Meyerowitz 1991). Genes A (APETALA 1, AP1; AP2; CAULIFLOWER, CAL; FRUITFUL, FUL) specify sepal formation in whorl 1; genes A and B (AP3; PISTILLATA, PI) act together to specify petal formation in whorl 2; genes B and C (AGAMOUS, AG) act together to specify stamen formation in whorl 3; gene C acts alone to specify carpel formation in whorl 4; the functions of genes A and C are mutually inhibitory (Coen and Meyerowitz 1991; Weige and Meyerowitz 1994) . The revised ‘ABCDE model’ stated that D genes (AG, SHATTERPROOF 1, SHP1; SHP2; SEEDSTICK, STK) are solely responsible for ovule identity and that E genes (SEPALLATA 1, SEP1; SEP2; SEP3; SEP4) combine with A, B, C, and D genes in five types of combinations (A ? E, A ? B ? E, B ? C ? E, C ? E, and D ? E) to specify sepal, petal, stamen, carpel, and ovule formation, respectively (Theißen et al. 2000; Pelaz et al. 2000, 2001; Theißen 2001; Theißen and Saedler 2001; Pinyopich et al. 2003; Krizek and Fletcher 2005; Bortiri and Hake 2007; Thompson and Hake 2009) (Fig. 2a). According to ‘ABCDE model’, we can get some key components: (1) MADS-box genes independently regulate their target organs development; (2) one or a class of genes expressed in one or more whorls; and (3) the development of one whorl floret organ is usually controlled by several classes of genes (Krizek and Fletcher 2005) . Furthermore, combinations of different functioning proteins encoded by homeotic genes regulate their upstream and downstream genes (Lenhard et al. 2001; Lohmann et al. 2001) . For example, a combination of LEAFY (LFY), API, and UNUSUAL FLORAL ORGANS (UFO) proteins initiates AP3 expression in whorl 2/3 organs, and a protein complex of LFY and WUSCHEL (WUS) is pivotal to AG expression in whorl 3/4 organs (Lenhard et al. 2001; Lohmann et al. 2001; Ng and Yanofsky 2001a, b; Favaro et al. 2003) . And a ‘quartet model’ of flower organ identity has been proposed to reflect the combinations of four different floral homeotic proteins encoded by floral organ identity genes (Theißen 2001; Theißen and Saedler 2001) (Fig. 2b). A large number of Arabidopsis floral identity orthologues that encode A, B, C, D, and E proteins have been found in maize (Fischer et al. 1995; Theissen et al. 1995; Cacharro´n et al. 1999; McSteen et al. 2000; Heuer et al. 2001; Ng and Yanofsky 2001a, b; Mu¨nster et al. 2001 , 2002; Lid et al. 2004; Schreiber et al. 2004 ; Whipple et al. 2004; Bommert et al. 2005a, b; Chuck et al. 2007; Palea, lemma, lodicule AP1 orthologue AP1 Leaf primordia, Young inflorescence – Stem node, egg cell Anther, lodicule primordia – – – – Carpel, anther Anther – Mature carpel – – Mature carpel – – Developing kernels and vegetative tissues – – UFM and floral organs SMs IM, floral primordia and pistil primordia SPMs, SMs, FMs FM, palea, lodicule, carpel, Carpel IMs, BMs, SPMs, FMs Inflorescence, ovule Early flowering CAL/FUL Promoting flowering Meristem gene, fertility AP3 orthologue PI orthologue AP1 PI AG orthologue AG STK orthologue STK orthologue AG SEP-like gene (SEP3) SEP-like gene (SEP1/2/4) Stamen development Pistil cell death Meristem gene – BMs enhancement – AGL2 – AP2 AGL6 TFL1/AG? AGL15 A B C D E – A? E? D? Mena et al. (1995) Danilevskaya et al. (2008) Mu¨nster et al. (2002) Heuer et al. (2001) Ambrose et al. (2000) Zhang et al. (2012) Whipple et al. (2004) Schmidt et al. (1993) Theissen et al. (1995) Mu¨nster et al. (2002) Schmidt et al. (1993) Theissen et al. (1995) Mu¨nster et al. (2002) Schmidt et al. (1993) Theissen et al. (1995) Mu¨nster et al. (2002) Lid et al. (2004) , Kobayashi et al. (2010) Kobayashi et al. (2010) Fischer et al. (1995) Cacharro´n et al. (1999) , Kobayashi et al. (2010) Kobayashi et al. (2010) Acosta et al. (2009), DeLong et al. (1993) Chuck et al. (2007) Mena et al. (1995) Gallavotti, et al. (2010) Zhang et al. (2012) 5 ‘–’, unknown content; ‘?’ undefined content) Gallavotti et al. 2010; Kobayashi et al. 2010; Zhang et al. 2012; Li et al. 2014) (Table 1). And the previous researches on silky 1 (si1), a maize female mutant, suggested that maize lemma and palea are homologous to Arabidopsis sepals, and that lodicules are homologous to petals (Ambrose et al. 2000; McSteen et al. 2000; Krizek and Fletcher 2005) (Fig. 2b). These research results indicate that the ‘ABCDE model’ also applies to maize flower (Whipple et al. 2004; Bommert et al. 2005a, b) (Fig. 2a). Like PI in Arabidopsis, gene Si1 possesses gene B functions, and specifies lodicule and stamen formation (Ambrose et al. 2000) . Zea mays MADS-box 4 (ZMM4) is an AP1-like gene that controls whorl 1/2 organs’ development. ZMM2 has a gene C function specifying anther formation (Schmidt et al. 1993; Danilevskaya et al. 2008) . The AG orthologous gene Zea AGAMOUS 1 (ZAG1) is thought to encode gene C proteins that determine stamen and carpel fate, and ZAG2 is a STK orthologue that contributes to ovule development (Schmidt et al. 1993) . The consummate study on beardedear (bde), a female mutant with multiple florets and organs in tassel and ear spikelets, especially silks from each spikelet, indicates that gene BDE shares E or SEP functions that regulate all four whorl floral organs’ development (Thompson et al. 2009) . According to sk1 phenotype that fails to produce ovules and silks in ear but with normal tassel and other organs, we speculate that gene SK1 is a pivotal contributor to D gene functions and specify ovule and silk formation (Jones 1925; Veit et al. 1993; Dellaporta and Calderon-Urrea 1994; Calderon-Urrea and Dellaporta 1999) . Sex-determining mutants affecting pistil development Feminization mutants Tassel seed mutants (tasselseeds 1, ts1; tasselseeds2, ts2; tasselseeds4, ts4; Tasselseeds3, Ts3; Tasselseeds 5, Ts5; Tasselseeds 6, Ts6) are typical feminization mutants and have very similar phenotype, characterized by viable kernels in the tassel and irregular rows of kernels in the ear (Emerson 1920; Jones 1934; Nickerson and Dale 1955; Veit et al. 1993) . In tassel florets, stamen development is inhibited and instead, pistils are formed, while in the ear, the pistils of lower floret survive through abortion stage as in tassel florets (Irish et al. 1994; Irish 1997; Chuck et al. 2007) . Exogenous jasmonic acid (JA) applied to the developing inflorescence of tassel seed mutants rescues the stamens, suggesting that JA plays a key role in stamen development (Acosta et al. 2009) . TASSEL SEED 1 (TS1) encodes a plastid-targeted lipoxygenase with putative 13-lipoxygenase activity, while TASSEL SEED 2 (TS2) shows significant protein sequence similarity to hydroxysteroid dehydrogenases, which suggests that both TS1 and TS2 contribute to JA biosynthetic pathway (DeLong et al. 1993; Acosta et al. 2009) . TASSELSEED 4 (TS4) encodes a microRNA, mir172, which targets AP2 floral homeotic transcription factors, implying a negative regulatory role in specifying maize floral organ identity (Chuck et al. 2007) (Fig. 4b). Dwarf mutant nana plant 1 (na1) and required to maintain repression 6 (rmr6) share a similar phenotype with tassel seed mutants (Parkinson et al. 2007; Hartwig et al. 2011) (Table 2). Brassinosteroid (BR) biosynthesis inhibitors enhance na1 phenotype, implying that the dwarfism and tassel seed phenotype of na1 are caused by a BR deficiency (Hartwig et al. 2011). NANA PLANT 1 (NA1) defects greatly reduce endogenous BR levels, indicating that NA1 plays important roles in BR biosynthetic pathway (Hartwig et al. 2011) . rmr6 mutants possess a feminized tassel that stamens in upper and lower florets are functional, which is the difference between rmr6 mutants and tassel seed mutants (Parkinson et al. 2007) . Required to maintain repression 6 (Rmr6) defines a novel tassel seed locus that differ from tassel seed mutations (Hollick et al. 2005; Parkinson et al. 2007) . The famous mutants, si1 and bde, share a similar phenotype (Fraser 1933; Ambrose et al. 2000; Thompson et al. 2009) . Scanning electron microscopy of the developing si1 spikelet shows that the anormogenesis of stamens primordia causes stamens developing into silks (Ambrose et al. 2000). bde encodes the MADS box gene previously described as zea agamous3 (zag3) and belongs to AGL6like family of MIKC-type transcription factors (Thompson et al. 2009) (Table 1). The similarity of bde with zag1 that produces extra carpels in ear florets and physical interaction of BDE and ZAG1 suggest that BDE and ZAG1 interact in a complex regulating floral organ number, and that BDE is also thought to function in other complexes that promote floral organ fate (Mena et al. 1995; Parenicova´ et al. 2003; Thompson et al. 2009) (Table 2). Masculinization mutants Anther-ear (An1) is a classical masculinizing dwarf mutant that has ears ending in thick unbranched tassel-like spikes with staminate florets only (Emerson and Emerson 1922) . Some An1 mutants show a phenotype that three well-developed stamens emerge from the ear spikelet resulting from a lack of normally developed silks, and the phenotype has a response to gibberellic acid (GA) (Bensen et al. 1995) . sk1 is an important female sterility mutant that has been studied for many years (Jones 1925, 1931, 1934) . A series of hybridization and backcross experiments using sk1 as the male and ts2 or normal progeny of sk1 as the female, implies an interaction between ts2 gene and sk1 gene (Jones 1934) . The rmr6/rmr6; sk1/sk1 double mutant bears no tassel seed, demonstrating that sk1 is epistatic to rmr6 and ectopic SK1 function as a pistil protector in rmr6 tassel florets (Parkinson et al. 2007) . Other sex mutants The ts4 and Ts6 mutations permit carpel development in the tassel while increasing meristem branching suggests that sex determination and acquisition of meristem fate may share a common pathway in maize. 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Studies of ra mutants demonstrate that RAMOSA2 (RA2) and RAMOSA3 (RA3) act upstream of RAMOSA1 (RA1) and combine with RA1 to repress ear branching, which creates a good example that MADS-box genes interact to regulate maize flower development (Eveland et al. 2014). Branched silkless (bd1) is a peculiar mutant, as like the union of ra mutant and sk1 (Kempton 1934; Colombo et al. 1998) (Table 2). In bd1 developing ear inflorescence, SMs often fail to initiate outer glumes and floret meristems, and directly initiate SPMs in a distichous phyllotaxy, resulting in branching. It is hypothesized that BDANCHED SILKLESS (BD1) gene products are required for SMs to convert into FMs (Chuck et al. 2002). Other sex mutants with defective pistil or silk development, such as zea agamous1 (zag1), thick tassel dwarf1 (td1), indeterminate floral apex1 (ifa1), knotted 1 (kn1), indeterminate spikelet 1 (ids1), and sterile tassel silky ear 1 (sts1), have a similar phenotype with tassel seed mutants and si1 or bde mutants, with crowded kernels in ear, a character that often results from a failure of pistils to abort in lower florets (Mena et al. 1996; Kerstetter et al. 1997; Chuck et al. 1998, 2008; Laudencia-Chingcuanco and Hake 2002; Young et al. 2004; Bommert et al. 2005a, b; Bolduc et al. 2012; Bartlett et al. 2015) (Table 2). Regulation of maize sex determination Previous research results of maize flower development suggested that pistil development and pistil meristem fate are controlled by a common pathway, in which low levels of cytokinin (CK) play important roles, and that endoplasmic reticulum-derived vesicles and vacuoles are involved (Calderon-Urrea and Dellaporta 1999; Balibrea Lara et al. 2004; Rogers 2006; Chuck et al. 2007; Kim et al. 2007) . Current knowledge of maize sex determination, as obtained by analysis of some sex-related mutants, is summarized in Fig. 3b, and the hypothetical genetic regulatory network, in Fig. 4. A detailed description of sex determination process is provided in the following sections, the functions and interactions of SK1, TS1, TS2, and sex-related locus Rmr6 are discussed as a key point. Phytohormones involved in sex determination Experiments on some andromonoecious dwarf mutants and tassel seed mutants imply that GA and JA play pivotal roles in maize sex determination (Dellaporta and Calderon-Urrea 1993, 1994; Spray et al. 1996; Calderon-Urrea and Dellaporta 1999; Kim et al. 2007) . Wild-type plants that are subjected to exogenous applications of GA often produce tassel seed, and endogenous GA, especially a high level of GA, protects the developing pistil and causes the stamens arrested (Nickerson 1959; Rood et al. 1980; Fujioka et al. 1988; Dellaporta and Calderon-Urrea 1994; Irish et al. 1994; Calderon-Urrea and Dellaporta 1999; Yamasaki et al. 2005) . The developing pistils immediately produce high levels of endogenous GA, which facilitates ovule and silk maturation (Dellaporta and Calderon-Urrea 1994; Eveland et al. 2014) . JA is required for stamen development and anther maturation in tassel (DeLong et al. 1993; Acosta et al. 2009) . BR is indicated to play crucial roles in stamen and anther development (Hartwig et al. 2011). CK is suggested to function in preventing pistil abortion after an experiment that transgenic plants expressing cytokininsynthesizing isopentenyl transferase (IPT) enzyme encoded by SAG12 (senescence associated gene 12) produce kernels Fig. 4 Determining process of pistil and stamen identity (modified from Dellaporta and Calderon-Urrea 1994; Yamasaki et al. 2005) . a The bisexual spikelet. b Sex-determining process in tassel florets. c Sex-determining process in ear florets. d The mature spikelet with unisexual florets. TFs transcription factors; dotted box possible physiological action, steel gray physiological action deficiency, and that have a fused endosperm with two viable embryos (Young et al. 2004). We propose that the roles of phytohormones are highly stage specific, and that the concentration of phytohormones affects their functions in sex determination (Yamaguchi and Kamiya 2000; Huang et al. 2003; Sakakibara 2006; Hirose et al. 2008; Pineda et al. 2008) . Here, we speculate that a relative high concentration of CK, BR, GA or JA contributes to promote the phytohormone functioning in pistil or stamen development and determining pistil or stamen fate. For example, although GA facilitates pistil development and conversely, arrests stamen, low levels of GA is still required for anthers and pollen formation in mature tassel florets (Yamasaki et al. 2005) . The interactions between CK, BR, GA, and JA are important parts of the regulatory network in sex determination. We propose that CK and GA either influence a common pathway or that CK upregulates GA biosynthesis at the critical stage of pistil development. A specific BR-biosynthesis inhibitor, the direct effect of the deficiency action to downstream actions burst deficiency; yellow box and barred lines the physiological action appear only under the over expression of the determining gene or when the effect from the upstream actions was excessive; ‘‘?’’ inferences need further examination Brz2001, is indicated similar to GA-biosynthesis inhibitor uniconazole, suggesting that BR and GA might share same substrate or enzyme in a similar biosynthetic pathway (Sekimata et al. 2001) . Researches on hormone signaling demonstrate that GA can induce MYB21/24 expression to activate the expression of various genes essential for JAregulated anther development and enhance JA/JA-lle synthesis (Song et al. 2010) . In Arabidopsis, certain levels of GA elevate JA/JA-lle levels by suppressing JA-biosynthesis inhibitory DELLA proteins to mobilize the expression of the JA-biosynthesis key gene DEFECTIVE ANTHER DEHISCENCE 1 (DAD1), which shares important auxiliary functions with auxin (Winkler and Freeling 1994; Cheng et al. 2009; Wasternack and Hause 2013) . Thus, we support that auxin may promote JA biosynthesis in developing tassel inflorescence meristems and floret meristems (Fig. 4b), and that it may combine with JA and promote anther development and pollen maturation (Gallavotti et al. 2008; Kieffer et al. 2010; Hartwig et al. 2012; Wasternack and Hause 2013; Yan et al. 2013; Galli et al. 2015) (Fig. 4b). In recent years, some other new phytohormones are found playing important roles in the regulation of floret organ development. For example, researches on the phylogenetic relationship and expression pattern of jasmonate ZIM-domain (JAZ) family genes has shown that ZmJAZ14 (referred to Zea mays Jasmonate ZIM-domain 14) gene may serve as a hub for the crosstalk between JA, abscisic acid (ABA), and GA signaling pathways in maize (Zhou et al. 2015) . And the main flavone O-glycosides biosynthetic enzyme gene ZmFNSI-1 (referred to maize FLAVONE SYNTHASEI-1) observed expresses at significantly higher levels in silks, suggesting a mysterious role of flavone in silk development (Ferreyra et al. 2015) . Functions of sex-determining genes It is indicated that TS2 produces pistil cell death signals, and that TS1 regulates TS2 expression by controlling the synthesis and accumulation of TS2 mRNA in pistil cells (Calderon-Urrea and Dellaporta 1999) . Calderon-Urrea and Dellaporta proposed a model in which SK1 only expresses in upper florets of ear and protects pistils from cell death signals by either restraining TS2 expression or blocking the downstream responders of TS2 products. GA is indicated to play key role in pistil (ovule and silk) development, therefore the silk absence of sk1 ear suggests that SK1 may play vital roles in GA biosynthesis or produce a pistilspecific factor (PSF) that promotes the pistils and inhibits the stamens (Jones 1925; Nickerson 1959; Calderon-Urrea and Dellaporta 1999; Yamasaki et al. 2005) . Also, the emergence of normal flowers in ts2/sk1 double mutants could suggest that TS2 may inhibit the developing pistils which are inferred to produce high levels of GA (Dellaporta and Calderon-Urrea 1994; Calderon-Urrea and Dellaporta 1999; Eveland et al. 2014) . Some na1 mutants accumulate (24R)-24-methylcholest-4-en-3-one with a concomitant decrease of downstream BR metabolites, which indicated that NA1 may encode a inhibition of (24R)-24-methylcholest-4-en-3-one accumulation with normal level of downstream BR metabolites (Hartwig et al. 2011). Studies on rmr6 mutants indicate that Rmr6 restricts SK1 activity in tassel florets and the lower florets of ear but not the upper florets of ear, and therefore is a key player in maize sex determination (Parkinson et al. 2007) . Other genes, such as TASSEL SEED 6 (TS6), Zeatin OGlucosyltransferase 1 (ZOG1), and IPT, may play specific roles in determining pistil fate (Fig. 4b). The research conclusions that gene ids1 is a key target gene of ts4, and that Ts6 mutants phenocopy ts4 and possess mutations in the microRNA binding site of ids1, demonstrate that TS6 is a target gene of TS4 and functions in inhibiting the pistil development in tassel floret development (Parkinson et al. 2007) . Maize plants transformed with a constitutively expressed ZOG1 gene from Phaseolus lunatus, which encodes a zeatin O-glucosyltransferase, have increased levels of active CK and feminized florets with small tassels, demonstrating that CK protects pistil cells from pistil cell death signals not only in the lower florets of ear but also in the tassel florets (Hirose et al. 2008) . Thus, IPT and ZOG1 are consistently connected with a high level of CK (Young et al. 2004; Hirose et al. 2008) (Fig. 4b, c). Determining process of sex determination In early development of tassel florets and ear lower florets, Rmr6 is required to restrain SK1 expression, which promotes stamens developing to maturity and pistil arrested (Parkinson et al. 2007) (Fig. 4b, c). In the upper floret of ear, Rmr6 expression might be blocked by a repressor or arrestin with a concomitant CK accumulation. Then, one hypothesis about the reason for pistil surviving from abortion is that higher levels of GA produced by SK1 combines with the CK and then restrain the synthetic pathway of cell death signals (Fig. 4c). Another hypothesis is that SK1 product directly blocks the cell death signals, or promotes PSF biosynthesis to protect pistils from the cell death signals (Fig. 4b, c). It was proposed that higher levels of GA produced by the developing pistils in ear upper floret might permeate through the lower floret and cause three stamens of lower floret arrested (Yamasaki et al. 2005) . The hypothesis about GA permeation from upper floret to lower floret of ear could be demonstrated by isotope labeling. And according to Jones’ observation that one of silkless (sk) mutants produce barren anthers in some of its cobs (Jones 1931, 1934) , we suggest to observe these unusual cobs and verify whether the stamens of lower florets survive from abortion and develop into anthers or not, which might also be conducive to validate Yamasaki hypothesis. Daher suggested that the earliest cellular indications of stamen arrest in tassel florets and the lower florets of ear are a cessation of cell division and precocious cell differentiation rather than cell death (Daher et al. 2010; Kim et al. 2007) . Kim et al. (2007) indicated that the cessation of cell division is determined by the detectable expression of gene CYCLINB, a G2/M regulator, and the accumulation of WEE1 RNA, a negative cell cycle regulator in arrested ear stamens. According to the results of Daher and Kim, we speculate that high levels of GA might be required for the cessation of pistil cell division or WEE1 successive expression, and that JA might be required for normal cell division in stamens and the cessation of cell division in pistil, and BR may be required for TS gene expression or eliminating the effects of GA on stamens development (Fig. 4b). Summary and future directions The various naturally occurring sex-related mutants of maize continue to offer excellent opportunities to study sex determination process. Understanding pistil development and sex determination process contributes to find new strategies to regulate maize flower development. The newly discovered sex-determining genes might be helpful to create maize male sterile lines for maize domestication and breeding work (Hake and Ross-Ibarra 2015) . It is well established that BR, CK, GA, and JA regulate floral organ development, and that the biosynthesis and functions of these phytohormones is regulated by both endogenous and environmental signals, especially light signaling (Huq 2006; Eveland and Jackson 2012) . However, SK1 has yet to be cloned and characterized and its mechanisms are unknown. And the functions of other sex-determining genes are also not very clear. For example, BD1 might act as an upstream regulatory gene in CK biosynthesis and, in doing so, elevates the expression of BDE, SI1, and SK1. Furthermore, movements of BR, CK, GA, and JA in the developing inflorescence, and the functions of auxin in sex determination are also poorly understood. To further understand the complex genetic regulatory network of maize sex determination, more sex-related genes especially SK1 need to be cloned and characterized, and the functions of more phytohormones also need to be clarified, especially the functions of auxin. Modern genetic tools such as genome-wide association mapping and genome-wide expression profiling analysis will accelerate these studies (Zhu et al. 2009; Yue et al. 2015) . And the signaling mechanisms and perception pathways of phytohormones are also important research directions (Lawit et al. 2010). Thorough investigations on the genetic regulatory network and signaling pathways of phytohormones in maize sex determination might shed light on the complex mechanisms of sex determination in other plants. Author contribution statement Q.L. and B.L. designed research; Q.L. collected documents and analyzed data; Q.L. and B.L. wrote the paper. Acknowledgments The author would like to acknowledge anonymous reviewers for helpful suggestions. Acosta IF , Laparra H , Romero SP , Schmelz E , Hamberg M , Mottinger JP , Moreno MA , Dellaporta SL ( 2009 ) tasselseed1 is a lipoxygenase affecting jasmonic acid signaling in sex determination of maize . 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Qinglin Li, Baoshen Liu. Genetic regulation of maize flower development and sex determination, Planta, 2017, 1-14, DOI: 10.1007/s00425-016-2607-2