Two imprinted genes primed by DEMETER in the central cell and activated by WRKY10 in the endosperm

The early development of the endosperm is crucial for balancing the allocation of maternal nutrients to offspring.This process is believed to be evolutionarily associated with genomic imprinting,resulting in parentally biased allelic gene expression.Beyond Fertilization Independent Seed(FIS)genes,the number of imprinted genes involved in early endosperm development and seed size determination remains limited.This study introduces early endosperm-expressed HAIKU(IKU)downstream Candidate F-box 1(ICF1)and ICF2 as maternally expressed imprinted genes(MEGs)in Arabidopsis thaliana.Although these genes are also demethylated by DEMETER(DME)in the central cell,their activation differs from the direct DME-mediated activation seen in classical MEGs such as the FIS genes.Instead,ICF maternal alleles carry pre-established hypomethylation in their promoters,priming them for activation by the WRKY10 transcription factor in the endosperm.On the contrary,paternal alleles are predominantly suppressed by CG methylation.Furthermore,we find that ICF genes partially contribute to the small seed size observed in iku mutants.Our discovery reveals a two-step regulatory mechanism that highlights the important role of conventional transcription factors in the activation of imprinted genes,which was previously not fully recognized.Therefore,the mechanism provides a new dimension to understand the transcriptional regulation of imprinting in plant reproduction and development.

Complex genetic architecture underlying the plasticity of maize agronomic traits

Phenotypic plasticity is the ability of a given genotype to produce multiple phenotypes in response to changing environmental conditions.Understanding the genetic basis of phenotypic plasticity and establishing a predictive model is highly relevant to future agriculture under a changing climate.Here we report findings on the genetic basis of phenotypic plasticity for 23 complex traits using a diverse maize population planted at five sites with distinct environmental conditions.We found that latituderelated environmental factors were the main drivers of across-site variation in flowering time traits but not in plant architecture or yield traits.For the 23 traits,we detected 109 quantitative trait loci(QTLs),29 for mean values,66 for plasticity,and 14 for both parameters,and 80%of the QTLs interacted with latitude.The effects of several QTLs changed in magnitude or sign,driving variation in phenotypic plasticity.We experimentally validated one plastic gene,ZmTPS14.1,whose effect was likely mediated by the compensation effect of ZmSPL6 from a downstream pathway.By integrating genetic diversity,environmental variation,and their interaction into a joint model,we could provide site-specific predictions with increased accuracy by as much as 9.9%,2.2%,and 2.6%for days to tassel,plant height,and ear weight,respectively.This study revealed a complex genetic architecture involving multiple alleles,pleiotropy,and genotype-byenvironment interaction that underlies variation in the mean and plasticity of maize complex traits.It provides novel insights into the dynamic genetic architecture of agronomic traits in response to changing environments,paving a practical way toward precision agriculture.

Transgenerational Inheritance and Resetting of Stress, Induced Loss of Epigenetic Gene Silencing in Arabidopsis

Plants, as sessile organisms, need to sense and adapt to heterogeneous environments and have developed sophisticated responses by changing their cellular physiology, gene regulation, and genome stability. Recent work dem- onstrated heritable stress effects on the control of genome stability in plants--a phenomenon that was suggested to be of epigenetic nature. Here, we show that temperature and UV-B stress cause immediate and heritable changes in the epi- genetic control of a silent reporter gene in Arabidopsis. This stress-mediated release of gene silencing correlated with pronounced alterations in histone occupancy and in histone H3 acetylation but did not involve adjustments in DNA meth- ylation. We observed transmission of stress effects on reporter gene silencing to non-stressed progeny, but this effect was restricted to areas consisting of a small number of cells and limited to a few non-stressed progeny generations. Further- more, stress-induced release of gene silencing was antagonized and reset during seed aging. The transient nature of this phenomenon highlights the ability of plants to restrict stress-induced relaxation of epigenetic control mechanisms, which likely contributes to safeguarding genome integrity.

LHP1 Interacts with ATRX through Plant-Specific Domains at Specific Loci Targeted by PRC2

Heterochromatin Protein 1 （HP1） is a major regulator of chromatin structure and function. In animals, the network of proteins interacting with HP1 is mainly associated with constitutive heterochromatin marked by H3K9me3. HP1 physically interacts with the putative ortholog of the SNF2 chromatin remodeler ATRX, which controls deposition of histone variant H3.3 in mammals. In this study, we show that the Arabidopsis thaliana ortholog of ATRX participates in H3.3 deposition and possesses specific conserved domains in plants. We found that plant Like HP1 （LHP1） protein interacts with ATRX through domains that evolved specifically in land plant ancestors. Loss of ATRX function in Arabidopsis affects the expression of a limited subset of genes controlled by PRC2 （POLYCOMB REPRESSIVE COMPLEX 2）, including the flowering time regulator FLC. The function of ATRX in regulation of flowering time requires novel LHPl-interacting domain and ATPase activity of the ATRX SNF2 helicase domain. Taken together, these results suggest that distinct evolutionary pathways led to the interaction between ATRX and HP1 in mammals and its counterpart LHP1 in plants, resulting in distinct modes of transcriptional regulation.

Ion Channels at the Nucleus： Electrophysiology Meets the Genome

The nuclear envelope is increasingly viewed from an electrophysiological perspective by researchers interested in signal transduction pathways that influence gene transcription and other processes in the nucleus. Here, we describe evidence for ion channels and transporters in the nuclear membranes and for possible ion gating by the nuclear pores. We argue that a systems-level understanding of cellular regulation is likely to require the assimilation of nuclear electrophysiology into molecular and biochemical signaling pathways.

H2A Variants in Arabidopsis: Versatile Regulators of Genome Activity

The eukaryotic nucleosome prevents access to the genome.Convergently evolving histone isoforms,also called histone variants,form diverse families that are enriched over distinct features of plant genomes.Among the diverse families of plant histone variants,H2A.Z exclusively marks genes.Here we review recent research progress on the genome-wide distribution patterns and deposition of H2A.Z in plants as well as its association with histone modifications and roles in plant chromatin regulation.We also discuss some hypotheses that explain the different findings about the roles of H2A.Z in plants.

Timing Is Everything： Highly Specific and Transient Expression of a MAP Kinase Determines Auxin-Induced Leaf Venation Patterns in Arabidopsis

Mitogen-activated protein kinase （MAPK） cascades are universal signal transduction modules present in all eukaryotes. In plants, MAPK cascades were shown to regulate cell division, developmental processes, stress responses, and hormone pathways. The subgroup A of Arabidopsis MAPKs consists of AtMPK3, AtMPK6, and AtMPK10. AtMPK3 and AtMPK6 are activated by their upstream MAP kinase kinases （MKKs） AtMKK4 and AtMKK5 in response to biotic and abiotic stress. In addition, they were identified as key regulators of stomatal development and patterning. AtMPKIO has long been considered as a pseudo-gene, derived from a gene duplication of AtMPK6. Here we show that AtMPKIO is expressed highly but very transiently in seedlings and at sites of local auxin maxima leaves. MPK10 encodes a functional kinase and interacts with the upstream MAP kinase kinase （MAPKK） AtMKK2. mpklO mutants are delayed in flowering in long-day conditions and in continuous light. Moreover, cotyledons of mpk10 and mkk2 mutants have reduced vein complexity, which can be reversed by inhibiting polar auxin transport （PAT）. Auxin does not affect AtMPKIO expression while treatment with the PAT inhibitor HFCA extends the expression in leaves and reverses the mpklO mutant phenotype. These results suggest that the AtMKK2-AtMPK10 MAPK module regulates venation complexity by altering PAT efficiency.

TOPLESS promotes plant immunity by repressing auxin signaling and is targeted by the fungal effector Naked1

In plants,the antagonism between growth and defense is hardwired by hormonal signaling.The perception of pathogen-associatedmolecularpatterns(PAMPs)frominvadingmicroorganismsinhibits auxin signalingand plant growth.Conversely,pathogens manipulate auxin signaling to promote disease,but how this hormone inhibits immunity is not fully understood.Ustilago maydis is a maize pathogen that induces auxin signaling in its host.We characterized a U.maydis effector protein,Naked1(Nkd1),that is translocated into the host nucleus.Through its native ethylene-responsive element binding factor-associated amphiphilic repression(EAR)motif,Nkd1 binds to the transcriptional co-repressors TOPLESS/TOPLESS-related(TPL/TPRs)and prevents the recruitment of a transcriptional repressor involved in hormonal signaling,leading to the derepression of auxin and jasmonate signaling and thereby promoting susceptibility to(hemi)biotrophic pathogens.A moderate upregulation of auxin signaling inhibits the PAMP-triggered reactive oxygen species(ROS)burst,an early defense response.Thus,our findings establish a clear mechanism for auxin-induced pathogen susceptibility.Engineered Nkd1 variants with increased expression or increased EAR-mediated TPL/TPR binding trigger typical salicylic-acid-mediated defense reactions,leading to pathogen resistance.This implies that moderate binding of Nkd1 to TPL is a result of a balancing evolutionary selection process to enable TPL manipulation while avoiding host recognition.

Regulation of floral senescence in Arabidopsis by coordinated action of CONSTANS and jasmonate signaling

In Arabidopsis,photoperiodic flowering is controlled by the regulatory hub gene CONSTANS(CO),whereas floral organ senescence is regulated by the jasmonates(JAs).Because these processes are chronologically ordered,it remains unknown whether there are common regulators of both processes.In this study,we discovered that CO protein accumulates in Arabidopsis flowers after floral induction,and it displays a diurnal pattern in floral organs different from that in the leaves.We observed that altered CO expression could affect flower senescence and abscission by interfering with JA response,as shown by petal-specific transcriptomic analysis as well as CO overexpression in JA synthesis and signaling mutants.We found that CO has a ZIM(ZINC-FINGER INFLORESCENCE MERISTEM)like domain that mediates its interaction with the JA response repressor JAZ3(jasmonate ZIM-domain 3).Their interaction inhibits the repressor activity of JAZ3,resulting in activation of downstream transcription factors involved in promoting flower senescence.Furthermore,we showed that CO,JAZ3,and the E3 ubiquitin ligase COI1(Coronatine Insensitive 1)could form a protein complex in planta,which promotes the degradation of both CO and JAZ3 in the presence of JAs.Taken together,our results indicate that CO,a key regulator of photoperiodic flowering,is also involved in promoting flower senescence and abscission by augmenting JA signaling and response.We propose that coordinated recruitment of photoperiodic and JA signaling pathways could be an efficient way for plants to chronologically order floral processes and ensure the success of offspring production.

Loss of two families of SPX domain-containing proteins required for vacuolar polyphosphate accumulation coincides with the transition to phosphate storage in green plants

Phosphorus is an essential nutrient for plants.It is stored as inorganic phosphate(Pi)in the vacuoles of land plants but as inorganic polyphosphate(polyP)in chlorophyte algae.Although it is recognized that the SPX-Major Facilitator Superfamily(MFS)and VPE proteins are responsible for Pi influx and efflux,respectively,across the tonoplast in land plants,the mechanisms that underlie polyP homeostasis and the transition of phosphorus storage forms during the evolution of green plants remain unclear.In this study,we showed that CrPTCI,encoding a protein with both SPX and SLC(permease solute carrier 13)domains for Pi transport,and CrVTC4,encoding a protein with both SPX and vacuolar transporter chaperone(VTC)domains for polyP synthesis,are required for vacuolar polyP accumulation in the chlorophyte Chlamydomonas rein-hardtii.Phylogenetic analysis showed that the SPX-SLC,SPX-VTC,and SPX-MFS proteins were present in the common ancestor of green plants(Viridiplantae).The SPX-SLC and SPX-VTC proteins are conserved among species that store phosphorus as vacuolar polyP and absent from genomes of plants that store phosphorus as vacuolar Pi.By contrast,SPX-MFS genes are present in the genomes of streptophytes that store phosphorus as Pi in the vacuoles.These results suggest that loss of SPX-SLC and SPX-VTC genes and functional conservation of SPX-MFS proteins during the evolution of streptophytes accompanied the change from ancestral polyP storage to Pi storage.