The Juvenile Phase of Maize Sees Upregulation of Stress-Response Genes and Is Extended by Exogenous Jasmonic Acid.

As maize (Zea mays) plants undergo vegetative phase change from juvenile to adult, they both exhibit heteroblasty, an abrupt change in patterns of leaf morphogenesis, and gain the ability to produce flowers. Both processes are under the control of microRNA156 (miR156), whose levels decline at the end of the juvenile phase. Gain of the ability to flower is conferred by the expression of miR156 targets that encode SQUAMOSA PROMOTER-BINDING transcription factors, which, when derepressed in the adult phase, induce the expression of MADS box transcription factors that promote maturation and flowering. How gene expression, including targets of those microRNAs, differs between the two phases remains an open question. Here, we compare transcript levels in primordia that will develop into juvenile or adult leaves to identify genes that define these two developmental states and may influence vegetative phase change. In comparisons among successive leaves at the same developmental stage, plastochron 6, three-fourths of approximately 1,100 differentially expressed genes were more highly expressed in primordia of juvenile leaves. This juvenile set was enriched in photosynthetic genes, particularly those associated with cyclic electron flow at photosystem I, and in genes involved in oxidative stress and retrograde redox signaling. Pathogen- and herbivory-responsive pathways including salicylic acid and jasmonic acid also were up-regulated in juvenile primordia; indeed, exogenous application of jasmonic acid delayed both the appearance of adult traits and the decline in the expression of miR156-encoding loci in maize seedlings. We hypothesize that the stresses associated with germination promote juvenile patterns of differentiation in maize.

The integration of leaf-derived signals sets the timing of vegetative phase change in maize, a process coordinated by epigenetic remodeling.

After germination, the maize shoot proceeds through a series of developmental stages before flowering. The first transition occurs during the vegetative phase where the shoot matures from the juvenile to the adult phase, called vegetative phase change (VPC). In maize, both phases exhibit easily-scored morphological characteristics, facilitating the elucidation of molecular mechanisms directing the characteristic gene expression patterns and resulting physiological features of each phase. miR156 expression is high during the juvenile phase, suppressing expression of squamosa promoter binding proteins/SBP-like transcription factors and miR172. The decline in miR156 and subsequent increase in miR172 expression marks the transition into the adult phase, where miR172 represses transcripts that confer juvenile traits. Leaf-derived signals attenuate miR156 expression and thus the duration of the juvenile phase. As found in other species, VPC in maize utilizes signals that consist of hormones, stress, and sugar to direct epigenetic modifiers. In this review we identify the intersection of leaf-derived signaling with components that contribute to the epigenetic changes which may, in turn, manage the distinct global gene expression patterns of each phase. In maize, published research regarding chromatin remodeling during VPC is minimal. Therefore, we identified epigenetic regulators in the maize genome and, using published gene expression data and research from other plant species, identify VPC candidates.

Jasmonic acid levels decline in advance of the transition to the adult phase in maize.

Leaf-derived signals drive the development of the shoot, eventually leading to flowering. In maize, transcripts of genes that facilitate jasmonic acid (JA) signaling are more abundant in juvenile compared to adult leaf primordia; exogenous application of JA both extends the juvenile phase and delays the decline in miR156 levels. To test the hypothesis that JA promotes juvenility, we measured JA and meJA levels using LC-MS in successive stages of leaf one development and in later leaves at stages leading up to phase change in both normal maize and phase change mutants. We concurrently measured gibberellic acid (GA), required for the timely transition to the adult phase. Jasmonic acid levels increased from germination through leaf one differentiation, declining in later formed leaves as the shoot approached phase change. In contrast, levels of GA were low in leaf one after germination and increased as the shoot matured to the adult phase. Multiple doses of exogenous JA resulted in the production of as many as three additional juvenile leaves. We analyzed two transcript expression datasets to investigate when gene regulation by miR156 begins in the context of spatiotemporal patterns of JA and GA signaling. Quantifying these hormones in phase change mutants provided insight into how these two hormones control phase-specific patterns of differentiation. We conclude that the hormone JA is a leaf-provisioned signal that influences the duration, and possibly the initiation, of the juvenile phase of maize by controlling patterns of differentiation in successive leaf primordia.