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The evolutionary dynamics and tissue specificity of protein-coding genes are well documented in plants. However, the evolutionary consequences of small RNAs (sRNAs) on tissue-specific functions remain poorly understood. Here, we performed integrated analysis of 195 deeply sequenced sRNA libraries of maize B73, representing more than 10 tissues, and identified a comprehensive list of 419 maize microRNA (miRNA) genes, 271 of which were newly discovered in this study. We further characterized the evolutionary dynamics and tissue specificity of miRNA genes and corresponding miRNA isoforms (isomiRs). Our analysis revealed that tissue specificity of isomiR events tends to be associated with miRNA gene abundance and suggested that the frequencies of isomiR types are affected by the local genomic regions. Moreover, genome duplication (GD) events have dramatic effect on evolutionary dynamics of maize miRNA genes, and the abundance divergence for tissue-specific miRNA genes is associated with GD events. Further study indicated that duplicate miRNA genes with tissue-specific expression patterns, such as miR2275a, a phased siRNA (phasiRNA) trigger, contribute to phenotypic traits in maize. Additionally, our study revealed the expression preference of 21- and 24-nt phasiRNAs in relation to tissue specificity. This large-scale sRNAomic study depicted evolutionary implications of tissue-specific maize sRNAs, which coordinate genome duplication, isomiR modification, phenotypic traits and phasiRNAs differentiation.

A large-scale bioinformatics analysis revealed the origin and evolution of GT47 gene family, and identified two clades of intron-poor genes with putative functions in drought stress responses and seed development in maize. Glycosyltransferase family 47 (GT47) genes encode β-galactosyltransferases and β-glucuronyltransferases that synthesize pectin, xyloglucans and xylan, which are important components of the plant cell wall. In this study, we performed a systematic and large-scale bioinformatics analysis of GT47 gene family using 352 GT47 proteins from 15 species ranging from cyanobacteria to seed plants. The analysis results showed that GT47 family may originate in cyanobacteria and expand along the evolutionary trajectory to moss. Further analysis of 47 GT47 genes in maize revealed that they can divide into five clades with diverse exon–intron structures. Among these five clades, two were mainly composed with intron-poor genes, which may originate in the moss. Gene duplication analysis revealed that the expansion of GT47 gene family in maize was significantly driven from tandem duplication events and segmental duplication events. Significantly, almost all duplicated genes are intron-poor genes. Expression analysis indicated that several intron-poor GT47 genes may be involved in the drought stress response and seed development in maize. This work provides insight into the origin and evolutionary process, expansion mechanisms and expression patterns of GT47 genes, thus facilitating their functional investigations in the future.

Crops are often subjected to periods of drought stress during their life cycle. However, how stress response mechanisms contribute to the crosstalk between stress signaling pathways and developmental signaling pathways is still unknown. We built a gene co-expression network from a spatio-temporal transcriptomic map of the drought stress response in maize (Zea mays), profiled from three tissues and four developmental stages and characterized hub genes associated with duplication events, selection, and regulatory networks. Co-expression analysis grouped drought-response genes into ten modules, covering 844 highly connected genes (hub genes). Of these, 15.4% hub genes had diverged by whole-genome duplication events and 2.5% might then have been selected during natural domestication and artificial improvement processes, successively. We identified key transcription factor hubs in a transcriptional regulatory network, which may function as a crosstalk mechanism between drought stress and developmental signalling pathways in maize. Understanding the evolutionary biases that have evolved to enhance drought adaptation lays the foundation for further dissection of crosstalk between stress signalling pathways and developmental signalling pathways in maize, towards molecular design of new cultivars with desirable yield and greater stress tolerance.

Cold acclimation is an important process by which plants respond to low temperature and enhance their winter hardiness. C-REPEAT BINDING FACTOR1 (CBF1), CBF2, and CBF3 genes were shown previously to participate in cold acclimation in Medicago truncatula In addition, MtCBF4 is transcriptionally induced by salt, drought, and cold stresses. We show here that MtCBF4, shown previously to enhance drought and salt tolerance, also positively regulates cold acclimation and freezing tolerance. To identify molecular factors acting upstream and downstream of the MtCBF4 transcription factor (TF) in cold responses, we first identified genes that are differentially regulated upon MtCBF4 overexpression using RNAseq Digital Gene Expression Profiling. Among these, we showed that MtCBF4 directly activates the transcription of the COLD ACCLIMATION SPECIFIC15 (MtCAS15) gene. To gain insights into how MtCBF4 is transcriptionally regulated in response to cold, an R2R3-MYB TF, MtMYB3, was identified based on a yeast one-hybrid screen as binding directly to MYB cis-elements in the MtCBF4 promoter, leading to the inhibition of MtCBF4 expression. In addition, another MYB TF, MtMYB61, identified as an interactor of MtMYB3, can relieve the inhibitory effect of MtMYB3 on MtCBF4 transcription. This study, therefore, supports a model describing how MtCBF4 is regulated by antagonistic MtMYB3/MtMYB61 TFs, leading to the up-regulation of downstream targets such as MtCAS15 acting in cold acclimation in M. truncatula.