Ms eye disc JH nutrition (comment by Leopold Layealle Science 2006)

American Association For The Advancement Of Science

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PERSPECTIVESDEVELOPMENT BIOLOGYEnvironmental cues affect the course of anLinking Nutrition and organism’s development. For example,in some insects, scarce nutrients induce ahormone to block tissue formation.Tissue GrowthPierre Léopold and Sophie Layalleomplex organisms must beMOLT METAMORPHOSISable to adapt their develop-Fourth instar larval stageCmental programs to ever- Fifth instar larval stagechanging environmental condi-MIFJHtions. One important way to coordi-nate this is through the use of hor-mones, regulatory molecules thatTimeexert diverse biological effects onmultiple and remote target tissues.In this context, juvenile hormoneJuvenile hormone (JH) A metamorphosis initiating factorhas fascinated insect endocrinolo-blocks proliferation of (MIF) induced by food stimulates gists for decades. This factor, pres-primordia cells. cell proliferation.ent in insects that undergo meta-Imaginal disc developmentmorphic changes during develop-ment, has many functions in orches-trating the insect life cycle, and thus Coordinating nutrition and hormone influence on tissue development. In the tobacco hornworm M. sexta, imaginalprovides an illuminating example disc tissue forms from primordia tissue late in larval development, after the fifth larval molt. This process is initiated by aof the kinds of pleiotropic effects signal of unknown nature called metamorphosis initiation factor, which is itself triggered by feeding. Shortly afterward,that hormones ...

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PERSPECTIVES

D E V E LO P M E N TB I O LO G Y Environmental cues affect the course of an Linking Nutrition and organism’s development. For example, in some insects, scarce nutrients induce a Tissue Growth hormone to block tissue formation. Pierre Léopold and Sophie Layalle omplex organisms must be MOLTMETAMORPHOSIS able to adapt their develop cha C nging environmental condi H MIF mental programs to ever Fifth Fourth instar larval stage instar larval stage J tions. One important way to coordi nate this is through the use of hor mones, regulatory molecules that Time exert diverse biological effects on multiple and remote target tissues. In this context, juvenile hormone Juvenile hormone (JH)A metamorphosis initiating factor has fascinated insect endocrinolo blocks proliferation of(MIF) induced by food stimulates gists for decades. This factor, pres primordia cells.cell proliferation. ent in insects that undergo meta Imaginal disc development morphic changes during develop ment, has many functions in orches trating the insect life cycle, and thus Coordinating nutrition and hormone influence on tissue development.In the tobacco hornwormM. sexta, imaginal provides an illuminating example disc tissue forms from primordia tissue late in larval development, after the fifth larval molt. This process is initiated by a of the kinds of pleiotropic effects signal of unknown nature called metamorphosis initiation factor, which is itself triggered by feeding. Shortly afterward, that hormones can have. Although it there is a decrease in the amount of circulating juvenile hormone. is known mostly for controlling (together with the steroid hormone ecdysone)to the discs via circulating systemic factors suchInterestingly, the normal persistence of juve molting during insect development, juvenileas insulinlike molecules and steroids (5hormone during the first day of the last). nile hormone also regulates organ morphogenesis,To enable the rapid increase in tissue masslarval instar stage in fed animals does not pre female fertility, adult behavior, diapause, andthat occurs during larval growth, larvae undergovent commitment of cells in the primordia to longevity (1,2). On page 1385 of this issue,a series of molts in which the cuticle is replaced.form late discs, suggesting that during the early Trumanet al. (3) add a new, key function to thisperiod of the fifth instar larva, the growthThese molts follow peaks of ecdysone produc list: relaying nutritional information to develoption that occur in the context of high concentrainhibitory effects of juvenile hormone are over ing tissues during insect development. Usingtions of juvenile hormone. During the last larvalridden by feeding. Indeed, locally applied the tobacco hornworm modelManduca sextapyriproxifen does not affect disc growth in feed, stage(the fifth instar), however, the concentration the authors provide compelling evidence thatof juvenile hormone drops, and the next molting late larvae. However, the dominance of feed juvenile hormone prevents the growth andchanges from a larvatolarva to a larvatopupaing over juvenile hormone appears to be development of future adult tissues in responsetransition (see the figure). Also, shortly beforerestricted to the last larval instar, because the to nutrient shortages during larval life.this, in the primordia tissue that develops late intohormone does block disc formation in younger M. sextafeeding animals. Thus, a nutritioninduced domimaginal discs, cells commit to metamorphosis, a pest for tobacco farmers, is a longtime lab star in the world of insect physioland undergo marked cell proliferation. This cominance factor appears to be produced early in the ogists. As in all holometabolous insects, themitment requires feeding, because complete starlast larval instar, allowing the imaginal disc pri adult organism, a moth, is produced from thevation of the animals during this period supmordia cells to commit to metamorphosis despite transformation of larval tissues called imaginalpresses disc formation (6). Interestingly, juvenilethe persistence of circulating juvenile hormone. discs (4). Imaginal discs are relatively simplehormone does not decline during the last larvalAs is often the case with novel and insightful structures that have served as a paradigm forstage in starved animals, suggesting that susfindings, the Trumanet al. work raises many understanding fundamental principles of develtained amounts of this hormone might be linkednew questions. The local effect of juvenile hor opment, such as the action of morphogeneticto the starvationinduced inhibition of disc formoneinduced growth inhibition suggests that molecules in establishing tissue polarity, as wellmation. In a key experiment, Truman and collabthe hormone might act cell autonomously on as the mechanisms coordinating patterning durorators suppressed juvenile hormone productiontarget tissues, directly affecting growth or pro ing tissue growth and differentiation. Previousin developing larvae by ablating their secretoryliferation in the cells of forming discs. The studies have found that imaginal tissue growthgland. In these animals, imaginal discs stillauthors provide evidence to support this, show is controlled by two primary factors: the patternformed, even under starvation conditions. Furthering that subnanomolar concentrations of pyri ing activity of morphogens, diffusible proteinsmore, locally treating the primordia of these larproxifen inhibit primordia cell proliferation. that organize fields of cells into distinct territovae with pyriproxifen, a compound that mimicsFurther deciphering the relevant molecular ries and define final tissue shapes; and environthe effects of juvenile hormone, efficientlyinteractions might be tricky though, because the mental cues like nutrition, which are conveyedrestored growth inhibition of imaginal disc tissue,signaling pathways downstream of juvenile hor showing that the hormone acts as a signal for starmone are poorly understood. vationinduced growth inhibition and that it doesIt will be equally important to determine how The authors are at CNRS/University of NiceSophia not need to be relayed by a systemic growthactithe nutritional sensing mechanism operates in Antipolis, UMR6543, Parc Valrose, 06108 Nice cedex 2, France. Email: [e-mail] vating molecule like insulin.Manducalarvae. The simplest mechanism could

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involve a nutritioninduced signal that would ren der each individual primordia cell insensitive to juvenile hormone–induced growth inhibition. This would not explain, however, why the same primordia cells are sensitive to juvenile hormone in earlystage feeding larvae but become resistant in the last instar. Alternatively, a signal that is dominant over juvenile hormone and that is trig gered by nutrition at this specific stage could do the job. The existence of such a “metamorphosis initiating factor” is suggested both by Truman et al. and by another recent study (7). Its nature and the mechanisms leading to its specific activa tion by nutrition at the start of the lastinstar larva remain to be identified. Finally, the sustained presence of juvenile hor mone in starved animals suggests that the endocrine tissue that produces this hormone might respond to nutrition and modulate its pro

duction or secretion accordingly. During food deprivation and in the absence of a metamorpho sis initiating factor, juvenile hormone would pre vent disc formation. Another possibility comes from recent studies inManduca’s cousin, the fruit flyDrosophila melanogaster, that implicate a larval tissue called the fat body (the equivalent of both vertebrate liver and fat tissue) in orchestrat ing nutritional responses (8,9).The larval fat body is an important source of juvenile hormone esterase, an enzyme that degrades the hormone to control its circulating levels. One possible sce nario is that the fat body, acting as a nutrition sen sor, modulates circulating amounts of juvenile hormone by producing the esterase and thereby directs imaginal disc development. The temporal control of this process is an intriguing issue that also needs to be addressed. Possible answers to these questions may come by extending these

P L A N TS C I E N C E Unfallen Grains: How Ancient Farmers Turned Weeds into Crops

John Doebley ome 10,000 years ago during the agricul tural revolution, ancient farmers bred hun cat S ed crops on which humans are dependent dreds of wild species into the domesti today. During this process, these ancient peoples saved seeds from plants with favored traits to form each subsequent generation, and over time they converted slender and unpromising wild species into reliable, bountiful crops. Variants or mutants of genes that conferred favorable phe notypes rose in frequency over time, while vari ants that best adapted plants to life in the wild were removed by selection from the domesti cated population. Foremost among the creations of ancient plant breeders are the cereals—rice, wheat, and maize, a triumvirate that provides more than 50% of the calories consumed by humans. As com pared to their progenitors, these cereals have more and larger grains, thicker stalks, seed that thresh freely from the chaff, and improved flavor. The cereals, and most other crops, share one additional feature that is central to domestication: Their grains remain attached to the plant for har vest by humans rather than falling (shattering) from the plant, as required for wild species to pro duce their next generation. Although quantitative trait locus (QTL) mapping (1) has convincingly shown that the evolution of domestication traits

The author is in the Laboratory of Genetics, University of Wisconsin, Madison, WI 53706, USA. Email: jdoebley@ wisc.edu

Gathering grain.Two agricultural workers harvest ing rice in Yangshuo, Guangxi Province, China.

such as the loss of shattering arose through a rel atively small number of gene changes, the nature of these genes and the molecular changes within them is not well understood. In research published inScienceearlier this year (2) and on page 1392 of this issue (3), groups in the United States and Japan take two

results to the genetically amenableDrosophila model, where new roles for juvenile hormone in development, growth, and morphogenesis are prime for exploration.

References 1. T.Flatt, M. P. Tu, M. Tatar,Bioessays27, 999 (2005). 2. L.I. Gilbert, N. A. Granger, R. M. Roe,Insect Biochem. Mol. Biol.30, 617 (2000). 3. J.W. Trumanet al.,Science312, 1385 (2006). 4. J.W. Truman, L. M. Riddiford,Nature401, 447 (1999). 5. S.J. Day, P. A. Lawrence,Development127, 2977 (2000). 6. S.G. MacWhinnieet al.,Dev. Biol.285, 285 (2005). 7. J.P. Allee, C. L. Pelletier, E. K. Fergusson, D. T. Champlin, J. Insect Physiol.52, 450 (2006). 8. J.S. Britton, B. A. Edgar,Development125, 2149 (1998). 9. J.Colombaniet al.,Cell114, 739 (2003).

10.1126/science.1128343

Cereals are the world’s primary food, but if they are to be harvested grains must remain on the plant. Two of the genetic changes responsible for this essential trait for domestication have been identified.

big steps toward bridging the gap between domestication QTLs and domestication genes. Liet al. (2) clonedshattering4(sh4), a gene first identified by this group as a major QTL control ling 69% of the variance for shattering in crosses of wild and cultivatedindicarice. This team was able to localize the causative difference to a 1700–base pair region, and then to demonstrate that a single amino acid change is principally responsible for the loss of shattering. An extraor dinary feature of the cultivated allele ofsh4is that it severely weakens but does not eliminate shattering. Thus, the grains are retained on the plants long enough for harvest, but then they can be removed easily by threshing. Konishiet al. (3) identified a second major shattering QTL (qSH1) in a cross of the two independently domesticated forms of rice,indica andjaponica. This QTL controls 68% of the variation for shattering in this hybrid population, and the authors cloned the gene and mapped the causative difference to a single nucleotide change. An absolutely exquisite result is that this single nucleotide change in cultivated rice obliterates a cisregulatory element required for the expres sion ofqSH1in the abscission layer, which is needed for the grain to break away from the plant. Other cisregulatory elements inqSH1are conserved between wild and cultivated rice, and thusqSH1still fulfills its other functions in the inflorescence of cultivated rice. These two rice genes join the growing num ber of plant domestication QTLs cloned to date.

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