INFLORESCENCE DEVELOPMENT IN TWO ANNUAL TEOSINTES: ZEA MAYS SUBSP. MEXICANA AND Z. MAYS SUBSP. PARVIGLUMIS

The ontogeny of tassels and ears in two annual Mexican teosintes, Zea mays subsp. mexicana and Z. mays subsp. parviglumis, was examined using scanning electron microscopy and light microscopy. Ear development in these annual teosintes follows a pattern previously described as leading to the bisexual mixed inflorescence in Z. diploperennis. Common bud primordia are initiated in the axils of distichously arranged bracts along the ear axis. These common primordia bifurcate to form paired sessile and pedicellate spikelet primordia. Development of pedicellate spikelets is arrested leaving the sessile spikelets, along with the adjoining rachis segment, to form solitary grains enclosed within cupulate fruitcases. Development of the central tassel spike is similar to that previously described in the Z. diploperennis tassel, except that the first formed axillary bud primordia form precocious tassel branches. The origin of these tassel branches suggests a possible mechanism for the transition from a distichous spike, characteristic of teosinte, to a polystichous spike, typical of maize.     

Analysis of inflorescence organogenesis in eastern gamagrass, Tripsacum dactyloides (Poaceae): the wild type and the gynomonoecious gsf1 mutant

Inflorescence organogenesis of a wild-type and a gynomonoecious (pistillate) mutant in Tripsacum dactyloides was studied using scanning electron microscopy. SEM (scanning electron microscope) analysis indicated that wild-type T. dactyloides (Eastern gamagrass) expressed a pattern of inflorescence organogenesis that is observed in other members of the subtribe Tripsacinae (Zea: maize and teosinte), family Poaceae. Branch primordia are initiated acropetally along the rachis of wild-type inflorescences in a distichous arrangement. Branch primordia at the base of some inflorescences develop into long branches, which themselves produce an acropetal series of distichous spikelet pair primordia. All other branch primordia function as spikelet pair primordia and bifurcate into pedicellate and sessile spikelet primordia. In all wild-type inflorescences development of the pedicellate spikelets is arrested in the proximal portion of the rachis, and these spikelets abort, leaving two rows of solitary sessile spikelets. Organogenesis of spikelets and florets in wild-type inflorescences is similar to that previously described in maize and the teosintes. Our analysis of gsf1 mutant inflorescences reveals a pattern of development similar to that of the wild type, but differs from the wild type in retaining (1) the pistillate condition in paired spikelets along the distal portion of the rachis and (2) the lower floret in sessile spikelets in the proximal region of the rachis. The gsf1 mutation blocks gynoecial tissue abortion in both the paired-spikelet and the unpaired-spikelet zone. This study supports the hypothesis that both femaleness and maleness in Zea and Tripsacum inflorescences are derived from a common developmental pathway. The pattern of inflorescence development is not inconsistent with the view that the maize ear was derived from a Tripsacum genomic background.     

Quantitative trait loci controlling phenotypes related to the perennial versus annual habit in wild relatives of maize

We used quantitative trait locus/loci (QTL) mapping to study the inheritance of traits associated with perennialism in a cross between an annual (Zea mays ssp. parviglumis) and a perennial (Z. diploperennis) species of teosinte. The most striking difference between these species is that Z. diploperennis forms rhizomes, whereas Z. mays ssp. parviglumis lacks these over-wintering underground stems. An F₂ population of 425 individuals was genotyped at 95 restriction fragment length polymorphism marker loci and the association between phenotype and genotype was analyzed by composite interval mapping. We detected a total of 38 QTL for eight traits. The number of QTL found for each trait ranged from two for rhizome formation to nine for tillering. QTL for six of the traits mapped near each other on chromosome 2, and QTL for four traits mapped near each other on chromosome 6, suggesting that these regions play an important role in the evolution of the perennial habit in teosinte. Most of the 38 QTL had small effects, and no single QTL showed a strikingly large effect. The map positions that we determined for rhizome formation and other traits in teosinte may help to locate corresponding QTL in pasture and turf grasses used as forage for cattle and for erosion control in agro-ecosystems.     

Development of the mixed inflorescence in Zea diploperennis litis, Doebley & Guzman (Poaceae)

Development of the mixed inflorescence in Zea diploperennis Iltis, Doebley & Guzman (Poaceae) Mixed inflorescences of diploperennial teosinte, which terminate the main branches of the plant, arise in the same fashion as tassel spikes. The apical meristem produces bracts in a decussate arrangement. A single axillary bud primordium is initiated in the axil of each bract. Growth of the bract is retarded as the bud enlarges and divides longitudinally into two separate spikelet primordia. The paired spikelets running in two ranks on either side of the inflorescence primordium produce the four-rowed condition typical of teosinte tasselS. In the transition region between male and female portions of the inflorescence, development of the pedicellate spikelet of each spikelet pair is arrested at an early ontogenetic stage. Continued growth of the sessile spikelet and associated rachis flaps destroy the remnants of the arrested spikelet in basal portions of the inflorescence. A similar abortion of the lower floret of the sessile spikelet results in a single pistillate floret per node at anthesis. These results provide further support for the hypothesis that a tassel-like mixed inflorescence of teosinte is ancestral to the maize ear.     

TAXONOMY OF ZEA (GRAMINEAE). I. A SUBGENERIC CLASSIFICATION WITH KEY TO TAXA

The genus Zea is here divided into the Sect. Luxuriantes Doebley & litis sect. n., including the perennials Z. diploperennis (2n = 20) and Z. perennis (2n = 40) and the annual Z. luxurians (2n = 20); and Sect. Zea , including the wild Z. mays ssp.parviglumis and Z. mays ssp. mexicana (both 2n = 20), and Z. mays ssp. mays (2n = 20), the highly domesticated and tremendously variable derivate of the latter. This division is verified by a multivariate analysis of a large number of morphological characters of the male inflorescence. Cytogenetic and chemotaxonomic evidence supports the morphological conclusions. A consideration of the phylogeny of Zea within the conceptual framework offered by this new sectioning of the genus points convincingly to annual teosinte (Z. mays ssp. mexicana) as the ancestor of cultivated maize.     

Early inflorescence and floral development in Zea mays land race Chapalote (Poaceae)

Tassel and ear primordia were collected from greenhouse-grown specimens of the Mexican maize landrace Chapalote and prepared for scanning electron microscopic (SEM) examination. Measurements of inflorescence apices and spikelet pair primordia (spp) were made from SEM micrographs. Correlation of inflorescence apex diameter with number of spikelet ranks showed no significant difference between tassels and ears, except at the two-rank level where the ear apical meristem had a significantly smaller diameter than corresponding two-ranked tassels. Within individual inflorescences, spp in different ranks enlarged at comparable rates, although the rates from one ear to the next along the stem differed. In both tassels and ears, spp divide to form paired sessile and pedicellate spikelet primordia when the spp is 150 μm wide; ear axes are significantly thicker than tassel axes at the time of bifurcation. The similarities in growth between ear and tassel primordia lend further support to the hypothesis that both the maize tassel and ear are derived from a common inflorescence pattern, a pattern shared with teosinte. Inflorescence primordial growth also suggests that a key character difference between teosinte and maize, distichous vs. polystichous arrangement of spikelets, may be related to size of the apical dome and/or rate of primordium production by the apical meristem. There appears to be more than a single morphological event in the shift from vegetative to reproductive growth. The evocation of axillary buds (ears) is independent of, and temporally separated from, the transition to flowering at the primary shoot apex (tassel).     

Inflorescence development in a new teosinte: Zea nicaraguensis (Poaceae)

Inflorescence development in a newly discovered teosinte, Zea nicaraguensis (Poaceae), from Nicaragua has been investigated using scanning electron microscopy (SEM). The SEM examination revealed that the pattern of both male and female inflorescence development was similar to previously described inflorescence in other Zea taxa. Branch primordia were initiated acropetally in a distichous pattern along the rachis of male and female inflorescences. Spikelet pair primordia bifurcated into pedicellate and sessile spikelet primordia. Predictably, pedicellate spikelet development was arrested and aborted in the female teosinte inflorescence. Organogenesis of functional spikelets and florets was similar to that previously described in maize and teosintes. The results were consistent with our hypothesis that both femininity and masculinity share a common mechanism of inflorescence development in Zea and Tripsacum and are in accord with a putative common mechanism of sex determination in the Andropogoneae. Interestingly, this population of teosinte, unique in its ability to grow in water-logged soils, showed a stable pattern of early inflorescence development. Our results also revealed the uncharacteristic presence of inflorescence polystichy in this population of Zea nicaraguensis. We propose this novel phenotypic variation raises the possibility that a domestic evolution of polystichy in maize was enabled by an occasional polystichous phenotypic in teosinte.     

Early ontogenetic development of the pistillate inflorescence in a diploid perennial teosinte (Zea diploperennis, Poaceae)

CAMARA-HERNANDEZ J. & GAMBINO, S., 1991. Early ontogenetic development of the pistillate inflorescence in a diploid perennial teosinte (Zea diploperennis , Poaceae). The early ontogeny of pistillate inflorescences of %ea diploperennis in plants grown at the latitude of Buenos Aires, Argentina, is investigated using the scanning electron microscope. The pattern of development of the inflorescence is similar to that in staminate and mixed inflorescences, starting with the formation of a pair of spikelets from a common branch primordium initiated in the axil of a bract on the ear axis. This bract arrests its development and aborts early. After initiation of an outer glume on both spikelet primordia, the pedicellate spikelet arrests its growth and aborts resulting in the mature inflorescence having two rows of solitary spikelets arranged distichally. This is significantly different from the pattern observed by other authors in plants grown in different environments (such as in natural populations in Mexico).     

Suppressor of sessile spikelets1 (Sosl): a dominant mutant affecting inflorescence development in maize

Suppressor of sessile spikeletsl (Sos1) is a dominant mutant of maize that blocks branching of the spikelet-pair primordium to form the sessile spikelet during ear development. As a result, Sos1 mutant ears and tassels possess single spikelets as opposed to the normal condition of paired spikelets, one sessile and the other pedicellate. Sos1 also causes a reduction in the number of tassel branches and the number of orthostichies (or cupule ranks) in the ear. The sos1 genetic locus maps to the short arm of maize chromosome 4. The Sos1 single spikelet phenotype appears similar to the single spikelet phenotype found in teosinte, the probable progenitor of maize. This similarity invites the hypothesis that sos1 had a role in the evolution of maize from teosinte. However, genetic mapping data and a comparison of the developmental basis of the single spikelet condition in the Sos1 mutant and teosinte demonstrate that their similar phenotypes result from distinct genetic-developmental mechanisms. These results indicate that sos1 was not involved in the evolution of maize and caution against drawing conclusions of homology based solely on similar adult phenotypes.     

Simple inheritance of key traits distinguishing maize and teosinte

The segregation of key traits distinguishing maize and teosinte was analyzed in three F₂ and three backcross populations derived from crosses of the modern maize inbred T232 withZea mays ssp.parviglumis. These traits were (i) paired vs. single female spikelets; (ii) two-ranked vs. many-ranked ears; (iii) non-indurated vs. indurated glumes; (iv) inclination of the kernels toward the rachis, and (v) distichous vs. polystichous central staminate spike. All traits showed a simple mode of inheritance except for paired female spikes, which appeared to be controlled by two genes. The loci controlling these major changes were mapped with RFLP markers to four chromosomal regions. These results support the suggestion that maize became differentiated from teosinte with as few as five major gene changes.This paper is dedicated to the memory of Professor Jean Pernes     

Molecular Evidence and the Evolution of Maize

In this review, the contributions of isozyme and chloroplast DNA studies to questions surrounding the evolution of maize are summarized. These methods of analysis provide generally strong support for the hierarchical system of classification of Zea proposed by Iltis and Doebley (1980). Molecular evidence is fully congruent with the theory that teosinte is ancestral to maize and suggests thatZ. mays subsp.parviglumis was the ancestral teosinte taxon. Further, these data show that only those populations from the central region of the range of subsp. parviglumis resemble maize in both isozymic and chloroplast DNA constitution. Presuming no major changes in the distribution of subsp. parviglumis since the domestication of maize, these data would place the origin of maize in the Balsas River drainage southwest of Mexico City. Molecular systematic evidence provides no support for theories that maize was domesticated independently several times; however, this type of data can not disprove such theories. Analyses of isozyme and chloroplast DNA diversity in Zea provide evidence of limited gene flow between maize and teosinte, but are not consistent with models that postulate extensive genetic interchange between these taxa. Isozyme studies have added substantially to the understanding of evolutionary relationships among extant races of maize and suggest that there are a small number of major racial complexes in Meso- and North America which have often evolved in response to environmental constraints associated with altitude. Ultimately, molecular genetic studies may allow a resolution of the controversy surrounding the morphological evolution of the maize ear.     

Expression patterns and mutant phenotype of teosinte branched1 correlate with growth suppression in maize and teosinte

The evolution of domesticated maize from its wild ancestor teosinte is a dramatic example of the effect of human selection on agricultural crops. Maize has one dominant axis of growth, whereas teosinte is highly branched. The axillary branches in maize are short and feminized whereas the axillary branches of teosinte are long and end in a male inflorescence under normal growth conditions. Previous QTL and molecular analysis suggested that the teosinte branched1 (tb1) gene of maize contributed to the architectural difference between maize and teosinte. tb1 mutants of maize resemble teosinte in their overall architecture. We analyzed the tb1 mutant phenotype in more detail and showed that the highly branched phenotype was due to the presence of secondary and tertiary axillary branching, as well as to an increase in the length of each node, rather than to an increase in the number of nodes. Double-mutant analysis with anther ear1 and tassel seed2 revealed that the sex of the axillary inflorescence was not correlated with its length. RNA in situ hybridization showed that tb1 was expressed in maize axillary meristems and in stamens of ear primordia, consistent with a function of suppressing growth of these tissues. Expression in teosinte inflorescence development suggests a role in pedicellate spikelet suppression. Our results provide support for a role for tb1 in growth suppression and reveal the specific tissues where suppression may occur.     

Molecular analysis of crosses between Tripsacum dactyloides and Zea diploperennis (Poaceae)

 DNA fingerprinting verified hybrid plants obtained by crossing Eastern gamagrass, Tripsacum dactyloides L., and perennial teosinte, Zea diploperennis Iltis, Doebley & R. Guzmán. Pistillate inflorescences on these hybrids exhibit characteristics intermediate to the key morphological traits that differentiate domesticated maize from its wild relatives: (1) a pair of female spikelets in each cupule; (2) exposed kernels not completely covered by the cupule and outer glumes; (3) a rigid, non-shattering rachis; (4) a polystichous ear. RFLP analysis was employed to investigate the possibility that traits of domesticated maize were derived from hybridization between perennial teosinte and Tripsacum. Southern blots of restriction digested genomic DNA of parent plants, F₁, and F₂ progeny from two different crosses were probed with RFLP markers specifically associated with changes in pistillate inflorescence architecture that signal maize domestication. Pairwise analysis of restriction patterns showed traits considered missing links in the origin of maize correlate with alleles derived from Tripsacum, and the same alleles are stably inherited in second generation progeny from crosses between Tripsacum and perennial teosinte. Received: 11 October 1996/Accepted:8 November 1996     

Molecular Evidence and the Evolution of Maize

In this review, the contributions of isozyme and chloroplast DNA studies to questions surrounding the evolution of maize are summarized. These methods of analysis provide generally strong support for the hierarchical system of classification of Zea proposed by Iltis and Doebley (1980). Molecular evidence is fully congruent with the theory that teosinte is ancestral to maize and suggests thatZ. mays subsp.parviglumis was the ancestral teosinte taxon. Further, these data show that only those populations from the central region of the range of subsp. parviglumis resemble maize in both isozymic and chloroplast DNA constitution. Presuming no major changes in the distribution of subsp. parviglumis since the domestication of maize, these data would place the origin of maize in the Balsas River drainage southwest of Mexico City. Molecular systematic evidence provides no support for theories that maize was domesticated independently several times; however, this type of data can not disprove such theories. Analyses of isozyme and chloroplast DNA diversity in Zea provide evidence of limited gene flow between maize and teosinte, but are not consistent with models that postulate extensive genetic interchange between these taxa. Isozyme studies have added substantially to the understanding of evolutionary relationships among extant races of maize and suggest that there are a small number of major racial complexes in Meso- and North America which have often evolved in response to environmental constraints associated with altitude. Ultimately, molecular genetic studies may allow a resolution of the controversy surrounding the morphological evolution of the maize ear.     

Pollination between maize and teosinte: an important determinant of gene flow in Mexico

Gene flow between maize [Zea mays (L.)] and its wild relatives does occur, but at very low frequencies. Experiments were undertaken in Tapachula, Nayarit, Mexico to investigate gene flow between a hybrid maize, landraces of maize and teosinte (Z. mays ssp. mexicana, races Chalco and Central Plateau). Hybridization, flowering synchrony, pollen size and longevity, silk elongation rates, silk and trichome lengths and tassel diameter and morphology were measured. Hybrid and open-pollinated maize ears produced a mean of 8 and 11 seeds per ear, respectively, when hand-pollinated with teosinte pollen, which is approximately 1–2% of the ovules normally produced on a hybrid maize ear. Teosinte ears produced a mean of 0.2–0.3 seeds per ear when pollinated with maize pollen, which is more than one-fold fewer seeds than produced on a maize ear pollinated with teosinte pollen. The pollination rate on a per plant basis was similar in the context of a maize plant with 400–500 seeds and a teosinte plant with 30–40 inflorescences and 9–12 fruitcases per inflorescence. A number of other factors also influenced gene-flow direction: (1) between 90% and 95% of the fruitcases produced on teosinte that was fertilized by maize pollen were sterile; (2) teosinte collections were made in an area where incompatibility systems that limit fertilization are present; (3) silk longevity was much shorter for teosinte than for maize (approx. 4 days vs. approx. 11 days); (4) teosinte produced more pollen on a per plant basis than the landraces and commercial hybrid maize; (5) teosinte frequently produced lateral branches with silks close to a terminal tassel producing pollen. Collectively these factors tend to favor crossing in the direction of teosinte to maize. Our results support the hypothesis that gene flow and the subsequent introgression of maize genes into teosinte populations most probably results from crosses where teosinte first pollinates maize. The resultant hybrids then backcross with teosinte to introgress the maize genes into the teosinte genome. This approach would slow introgression and may help explain why teosinte continues to co-exist as a separate entity even though it normally grows in the vicinity of much larger populations of maize.     

Population genetic structure of a specialist leafhopper on Zea: likely anthropogenic and ecological determinants of gene flow

Corn leafhopper, Dalbulus maidis DeLong & Wolcott (Hemiptera: Cicadellidae), is a specialist herbivore on the genus Zea (Poaceae). The genera Dalbulus and Zea evolved in central Mexico. We sought to determine whether population genetic structuring is prevalent in corn leafhoppers inhabiting three of its host plants: (1) the highland species perennial teosinte (Zea diploperennis Iltis, Doebley & Guzman), (2) the mid‐ to lowland‐species Balsas teosinte (Zea mays ssp. parviglumis Iltis & Doebley), and (3) the ubiquitous domesticated maize (Zea mays ssp. mays L.). We used amplified fragment length polymorphisms to detect population structuring and genetic differentiation among corn leafhoppers on the three host plants in western‐central and ‐northern Mexico. Our results showed that corn leafhopper in Mexico is composed of at least two genetically discrete populations: an ‘Itinerant’ population associated with the annual hosts maize and Balsas teosinte, which appears to be widely distributed in Mexico, and a ‘Las Joyas’ population restricted to perennial teosinte and confined to a small mountain range (Sierra de Manantlán) in western‐central Mexico. Our results further suggested that population structuring is not due to isolation by distance or landscape features: Las Joyas and Itinerant corn leafhopper populations are genetically distinct despite their geographic proximity (ca. 4 km), whereas Itinerant corn leafhoppers separated by hundreds of kilometers (>800 km), mountain ranges, and a maritime corridor (Sea of Cortez) are not genetically distinct. Based on our results and on published ethnohistorical and archaeological data, we propose pre‐Columbian and modern scenarios, including likely ecological and anthropogenic influences, in which the observed genetic population structuring of corn leafhopper could have originated and could be maintained. Also, we hypothesize that after evolving on the lowland Balsas teosinte, corn leafhopper expanded its host range to include maize and then the highland perennial teosinte, following the domestication and spread of maize within the last 9 000 years.     

Facilitated by nature and agriculture: performance of a specialist herbivore improves with host-plant life history evolution, domestication, and breeding

Plant defenses against herbivores are predicted to change as plant lineages diversify, and with domestication and subsequent selection and breeding in the case of crop plants. We addressed whether defense against a specialist herbivore declined coincidently with life history evolution, domestication, and breeding within the grass genus Zea (Poaceae). For this, we assessed performance of corn leafhopper (Dalbulus maidis) following colonization of one of four Zea species containing three successive transitions: the evolutionary transition from perennial to annual life cycle, the agricultural transition from wild annual grass to primitive crop cultivar, and the agronomic transition from primitive to modern crop cultivar. Performance of corn leafhopper was measured through seven variables relevant to development speed, survivorship, fecundity, and body size. The plants included in our study were perennial teosinte (Zea diploperennis), Balsas teosinte (Zea mays parviglumis), a landrace maize (Zea mays mays), and a hybrid maize. Perennial teosinte is a perennial, iteroparous species, and is basal in Zea; Balsas teosinte is an annual species, and the progenitor of maize; the landrace maize is a primitive, genetically diverse cultivar, and is ancestral to the hybrid maize; and, the hybrid maize is a highly inbred, modern cultivar. Performance of corn leafhopper was poorest on perennial teosinte, intermediate on Balsas teosinte and landrace maize, and best on hybrid maize, consistent with our expectation of declining defense from perennial teosinte to hybrid maize. Overall, our results indicated that corn leafhopper performance increased most with the agronomic transition, followed by the life history transition, and least with the domestication transition.     

Accurate documentation of Germplasm: The lost guatemalan teosintes (Zea,Gramineae)

The great need for adequate documentation of germplasm collections, including accurate geographic location, needs again to be stressed. We discuss 3 reported stations for teosinte (Zea spp., Gramineae) in Guatemala. The first was discovered by Melhus and Chamberlain in 1949; an attempt by the senior author to relocate this station in 1976 was unsuccessful, but we now have a good idea of where this population (probablyZ. luxurians) may occur. The second, that of Rojas in 1942, lies well outside the known ranges of either of the 2 Guatemalan teosintes, Z.luxurians andZ. mays subsp.parviglumis var.huehuetenangensis. The third, a collection of Steyermark’s, turns out to be aTripsacum. We urge plant scientists, applied botanists, geographers, anthropologists, and others to provide voucher specimens with accurate location data for all plant populations that they study.     

TAXONOMY OF ZEA (GRAMINEAE). II. SUBSPECIFIC CATEGORIES IN THE ZEA MAYS COMPLEX AND A GENERIC SYNOPSIS

A compromise classification of the genus Zea, reflecting both phylogeny and practical needs, recognizes six taxa, as follows: Section Luxuriantes : Zea perennis. Zea diploperennis, Zea luxurians. Section Zea : Zea mays ssp. mexicana (Neo-volcanic Plateau), Zea mays ssp. parviglumis Iltis & Doebley ssp. n. var. parviglumis (Rio Balsas drainage, Pacific slope from Guerrero to Jalisco), Zea mexicana ssp. parviglumis var. huehuetenangensis Iltis & Doebley var. n. (Pacific slope, western Guatemala, Prov. Huehuetenango), Zea mays ssp. mays. The new subspecies is distinguished by smaller spikelets and rachis joints, the varieties by different habitats, blooming dates and their genetic behavior in relation to cultivated Zea mays. Zea mays ssp. mexicana is the ancestor of corn.