Title: Transcriptional corepressors in maize maintain meristem development
Abstract
The formation of the plant body proceeds in a sequential postembryonic manner through the action of meristems. Tightly coordinated meristem regulation is required for development and reproductive success, eventually determining yield in crop species. In maize (Zea mays), the RAMOSA1 ENHANCER LOCUS2 (REL2) family of transcriptional corepressors includes four members, REL2, RELK1 (REL2-LIKE1), RELK2, and RELK3. In a screen for rel2 enhancers, we identified shorter double mutants with enlarged ear inflorescence meristems (IMs) carrying mutations in RELK1. Expression and genetic analysis indicated that REL2 and RELK1 cooperatively regulate ear IM development by controlling genes involved in redox balance, hormone homeostasis, and differentiation, ultimately tipping the meristem toward an environment favorable to expanded expression of the ZmWUSCHEL1 gene, which encodes a key stem-cell promoting transcription factor. We further demonstrated that RELK genes have partially redundant yet diverse functions in the maintenance of various meristem types during development. By exploiting subtle increases in ear IM size in rel2 heterozygous plants, we also showed that extra rows of kernels are formed across a diverse set of F1 hybrids. Our findings reveal that the REL2 family maintains development from embryonic initiation to reproductive growth and can potentially be harnessed for increasing seed yield in a major crop species.
The formation of the plant body proceeds in a sequential post-embryonic manner through the action of meristems. Tightly coordinated meristem regulation is required for development and reproductive success, eventually determining yield in crop species. In maize, the REL2 family of transcriptional corepressors includes four members, REL2, RELK1 (REL2-LIKE1), RELK2, and RELK3. In a screen forrel2enhancers, we identified shorter double mutants with enlarged female inflorescence meristems (IMs) carrying mutations inRELK1. Expression and genetic analysis indicate thatREL2andRELK1cooperatively regulate female IM development by controlling genes involved in redox balance, hormone homeostasis, and differentiation, ultimately tipping the meristem toward an environment favorable to expanded expression of theZmWUSCHEL1gene, a key stem-cell promoting transcription factor. We further demonstrate thatRELKgenes have partially redundant yet diverse functions in the maintenance of various meristem types during development. By exploiting subtle increases in ear IM size inrel2heterozygous plants, we also show that extra rows of kernels are formed across a diverse set of F1 hybrids. Our findings reveal that the REL2 family maintains development from embryonic initiation to reproductive growth and can potentially be harnessed for increasing seed yield in a major crop species.
One sentence summary
REL2-RELKs fine tune hormone and chemical cues to prevent expanded expression of ZmWUSCHEL1 in maize inflorescence meristems, and can potentially be harnessed for increasing seed yield in hybrids.
Du, Yanfang; Lunde, China; Li, Yunfu; Jackson, David; Hake, Sarah; Zhang, Zuxin(
, Proceedings of the National Academy of Sciences)
null
(Ed.)
Plant meristems are self-renewing groups of pluripotent stem cells that produce lateral organs in a stereotypical pattern. Of interest is how the radially symmetrical meristem produces laminar lateral organs. Both the male and female inflorescence meristems of the dominant Fascicled ear ( Fas1 ) mutant fail to grow as a single point and instead show deep branching. Positional cloning of two independent Fas1 alleles identified an ∼160 kb region containing two floral genes, the MADS-box gene, zmm8 , and the YABBY gene, drooping leaf2 ( drl2 ). Both genes are duplicated within the Fas1 locus and spatiotemporally misexpressed in the mutant inflorescence meristems. Increased zmm8 expression alone does not affect inflorescence development; however, combined misexpression of zmm8 , drl2 , and their syntenic paralogs zmm14 and drl1 , perturbs meristem organization. We hypothesize that misexpression of the floral genes in the inflorescence and their potential interaction cause ectopic activation of a laminar program, thereby disrupting signaling necessary for maintenance of radially symmetrical inflorescence meristems. Consistent with this hypothesis, RNA sequencing and in situ analysis reveal altered expression patterns of genes that define distinct zones of the meristem and developing leaf. Our findings highlight the importance of strict spatiotemporal patterns of expression for both zmm8 and drl2 and provide an example of phenotypes arising from tandem gene duplications.
A fascinating feature of land plants is their ability to continually initiate new tissues and organs throughout their lifespan, driven by a pool of pluripotent stem cells located in meristems. In seed plants, various types of meristems are initiated and maintained during the sporophyte generation, while their gametophytes lack meristems and rely on sporophyte tissues for growth. In contrast, seed‐free vascular plants, such as ferns, develop meristems during both the sporophyte and gametophyte generations, allowing for the independent growth of both generations. Recent findings have highlighted both conserved and lineage‐specific roles of the HAIRY MERISTEM (HAM) family of GRAS‐domain transcriptional regulators in various meristems throughout the land plant lifecycle. Here, we review and discuss howHAMgenes maintain meristem indeterminacy in both sporophytes and gametophytes, with a focus on studies performed in two model species: the flowering plantArabidopsis thalianaand the fernCeratopteris richardii. Additionally, we summarize the crucial and tightly regulated functions of the microRNA171 (miR171)‐HAM regulatory modules, which define HAM spatial patterns and activities during meristem development across various meristem identities in land plants.
Chu, Yi‐Hsuan; Jang, Jyan‐Chyun; Huang, Zejun; van der Knaap, Esther(
, Plant Direct)
Abstract
Improving yield by increasing the size of produce is an important selection criterion during the domestication of fruit and vegetable crops. Genes controlling meristem organization and organ formation work in concert to regulate the size of reproductive organs. In tomato,lcandfascontrol locule number, which often leads to enlarged fruits compared to the wild progenitors.LCis encoded by the tomato ortholog ofWUSCHEL(WUS), whereasFASis encoded by the tomato ortholog ofCLAVATA3 (CLV3). The critical role of theWUS‐CLV3 feedback loop in meristem organization has been demonstrated in several plant species. We show that mutant alleles for both loci in tomato led to an expansion of theSlWUSexpression domain in young floral buds 2–3 days after initiation. Single and double mutant alleles oflcandfasmaintain higherSlWUSexpression during the development of the carpel primordia in the floral bud. This augmentation and altered spatial expression ofSlWUSprovided a mechanistic basis for the formation of multilocular and large fruits. Our results indicated thatlcandfasare gain‐of‐function and partially loss‐of‐function alleles, respectively, while both mutations positively affect the size of tomato floral meristems. In addition, expression profiling showed thatlcandfasaffected the expression of several genes in biological processes including those involved in meristem/flower development, patterning, microtubule binding activity, and sterol biosynthesis. Several differentially expressed genes co‐expressed withSlWUShave been identified, and they are enriched for functions in meristem regulation. Our results provide new insights into the transcriptional regulation of genes that modulate meristem maintenance and floral organ determinacy in tomato.
Geng, Yuan; Guo, Lei; Han, Han; Liu, Xing; Banks, Jo Ann; Wisecaver, Jennifer H.; Zhou, Yun(
, The Plant Journal)
SUMMARY
The shoot apical meristems (SAMs) of land plants are crucial for plant growth and organ formation. In several angiosperms, theHAIRY MERISTEM(HAM) genes function as key regulators that control meristem development and stem cell homeostasis. To date, the origin and evolutionary history of the HAM family in land plants remains unclear. Potentially shared and divergent functions of HAM family members from angiosperms and non‐angiosperms are also not known. In constructing a comprehensive phylogeny of the HAM family, we show that HAM proteins are widely present in land plants and that HAM proteins originated prior to the divergence of bryophytes. The HAM family was duplicated in a common ancestor of angiosperms, leading to two distinct groups: type I and type II. Type‐II HAM members are widely present in angiosperms, whereas type‐I HAM members were independently lost in different orders of monocots. Furthermore, HAM members from angiosperms and non‐angiosperms (including bryophytes, lycophytes, ferns and gymnosperms) are able to replace the role of the type‐IIHAMgenes in Arabidopsis, maintaining established SAMs and promoting the initiation of new stem cell niches. Our results uncover the conserved functions of HAM family members and reveal the conserved regulatory mechanisms underlying HAM expression patterning in meristems, providing insight into the evolution of key stem cell regulators in land plants.
@article{osti_10544204,
place = {Country unknown/Code not available},
title = {Transcriptional corepressors in maize maintain meristem development},
url = {https://par.nsf.gov/biblio/10544204},
DOI = {10.1093/plphys/kiae476},
abstractNote = {Abstract The formation of the plant body proceeds in a sequential postembryonic manner through the action of meristems. Tightly coordinated meristem regulation is required for development and reproductive success, eventually determining yield in crop species. In maize (Zea mays), the RAMOSA1 ENHANCER LOCUS2 (REL2) family of transcriptional corepressors includes four members, REL2, RELK1 (REL2-LIKE1), RELK2, and RELK3. In a screen for rel2 enhancers, we identified shorter double mutants with enlarged ear inflorescence meristems (IMs) carrying mutations in RELK1. Expression and genetic analysis indicated that REL2 and RELK1 cooperatively regulate ear IM development by controlling genes involved in redox balance, hormone homeostasis, and differentiation, ultimately tipping the meristem toward an environment favorable to expanded expression of the ZmWUSCHEL1 gene, which encodes a key stem-cell promoting transcription factor. We further demonstrated that RELK genes have partially redundant yet diverse functions in the maintenance of various meristem types during development. By exploiting subtle increases in ear IM size in rel2 heterozygous plants, we also showed that extra rows of kernels are formed across a diverse set of F1 hybrids. Our findings reveal that the REL2 family maintains development from embryonic initiation to reproductive growth and can potentially be harnessed for increasing seed yield in a major crop species.},
journal = {Plant Physiology},
publisher = {Oxford University Press},
author = {Gregory, Jason and Liu, Xue and Chen, Zongliang and Gallardo, Cecilia and Punskovsky, Jason and Koslow, Gabriel and Galli, Mary and Gallavotti, Andrea},
}
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