Moderate drought causes dramatic floral transcriptomic reprogramming to ensure successful reproductive development in Arabidopsis
© Ma et al.; licensee BioMed Central Ltd. 2014
Received: 15 February 2014
Accepted: 29 May 2014
Published: 13 June 2014
Drought is a major constraint that leads to extensive losses to agricultural yield worldwide. The potential yield is largely determined during inflorescence development. However, to date, most investigations on plant response to drought have focused on vegetative development. This study describes the morphological changes of reproductive development and the comparison of transcriptomes under various drought conditions.
The plants grown were studied under two drought conditions: minimum for successful reproduction (45-50% soil water content, moderate drought, MD) and for survival (30-35%, severe drought, SD). MD plants can produce similar number of siliques on the main stem and similar number of seeds per silique comparing with well-water plants. The situation of SD plants was much worse than MD plants. The transcriptomes of inflorescences were further investigated at molecular level using microarrays. Our results showed more than four thousands genes with differential expression under severe drought and less than two thousand changed under moderate drought condition (with 2-fold change and q-value < 0.01). We found a group of genes with increased expression as the drought became more severe, suggesting putative adaptation to the dehydration. Interestingly, we also identified genes with alteration only under the moderate but not the severe drought condition, indicating the existence of distinct sets of genes responsive to different levels of water availability. Further cis-element analyses of the putative regulatory sequences provided more information about the underlying mechanisms for reproductive responses to drought, suggesting possible novel candidate genes that protect those developing flowers under drought stress.
Different pathways may be activated in response to moderate and severe drought in reproductive tissues, potentially helping plant to maximize its yield and balance the resource consumption between vegetative and reproductive development under dehydration stresses.
KeywordsModerate drought Severe drought Reproductive development Transcriptome Arabidopsis
The increasing world population (up to 7 billion in 2010) suggests a growing demand in crop production. Agricultural productivity is inevitably impacted by environmental stresses, such as drought, salinity, heat and cold . Many of these abiotic factors can cause loss of yields partially resulting from dehydration of plant cells. Despite the abundance of water on earth, most of the water resources are not usable for irrigation due to salinity. Thus, an increasing number of investigations has focused on the mechanisms enabling plants adaptation to dehydration. Dehydration resistance consists of two main categories: dehydration avoidance or dehydration tolerance . Dehydration avoidance is defined as the plant capacity to maintain cellular hydration in spite of stress and plants could achieve it by maintaining soil moisture, limiting water use (WU), and osmotic adjustment (OA). Dehydration tolerance is defined as the relative capacity to maintain normal function even in a (partially) dehydrated state, which is also viewed as a secondary defense against desiccation. This mechanism is not commonly observed other than in seed embryo and the only main exception occurs during certain stages of grain filling under drought .
Drought, the most direct reason leading to plant dehydration, has been studied for years. It could impact plants at molecular, cellular, physiological and biochemical levels and can severely affect multiple developmental process, including seed germination , seedling growth , root development  and later leaf development [7–9]. In many flowering plants, the emergence of flowers coincides with drought stress during summer. To ensure successful reproduction, flowering plant must possess mechanisms that protect flowers from severe dehydration. However, only a few studies have examined reproductive development under drought conditions at molecular level [10, 11].
Another challenge for scientists studying drought is how to control water availability. It is known from both agricultural experience and experimental studies that varying degrees of water shortage could impact crop development and yield to different extents . A few studies tried to calculate the minimum water requirement in certain regions and proposed to enhance the capacity in dealing with drought using water management [13, 14]. However, field studies on drought potentially have substantial limitation for several reasons: 1) the difficulty of controlling soil water content accurately; 2) delay of drought effects on plant due to the variation of evaporation rate and soil content; and 3) substantial deviation due to variation of nutrients in soil. Therefore, it is difficult to estimate the minimum water requirement for plant survival or fertility from field studies.
On the other hand, studies in the lab could allow relatively accurate control of the water amounts to explore the mechanisms that plants employ to survive. By reducing the water supply, many genes have been found to be involved in complex drought responses, including both ABA-dependent and ABA-independent drought-responsive pathways [1, 15, 16]. Further studies revealed additional key components in these pathways, including transcription factors belonging to the bZIP, AP2/ERF, and MYB families [17–19]. With the help of transcriptomic profiling, more and more drought-responsive genes have been reported, especially in the model plants whose genomic information is available, such as Arabidopsis, rice and maize [1, 20, 21]. However, those studies often focused on vegetative tissues [20, 22].
A recent study in our lab has shown the impacts of severe drought on reproductive development, such as reduced flower number and size, and fewer seeds . In addition, detailed morphological analyses showed that the development of both male and female reproductive organs was affected by drought, resulting in ovule abortion, failure of flowers to open, abnormal anther development and delayed elongation of the filaments and stigmatic papillae cells. Further examination of the inflorescence transcriptomes under well-watered and severe drought conditions indicated that the floral transcriptome underwent dramatic reprogramming during severe drought treatment . However, as only severe drought was applied in the previous study, it was not clear what are the effects of different extent of drought stresses on reproductive development and transcriptomes.
Here, to understand the impacts of different magnitude of drought stress on reproductive development, we treated the Arabidopsis plants with different drought severities soon after the bolting stage (around the time of the first opening flower) and observed their morphological changes. We further investigated the changes of inflorescence transcriptome under a moderate degree of drought. We collected inflorescences from treated plants at different times after moderate drought treatment and used the mRNA samples from the inflorescences for microarray experiments. The differential gene expression patterns were combined with promoter cis-acting element analysis to provide further understanding of flower development in response to moderate and severe drought stresses. We propose that many genes important for flower development are responsive to drought to protect reproductive success to some extent under drought stress.
Morphological changes of Arabidopsisflowers in response to drought of different severities
We had previously found that the reproductive yield was sensitive to severe drought conditions . To learn the effects of moderate drought conditions, we counted the seed number per seedpod and found that plants could endure slight to moderate drought without obvious reduction in seed number on the main stem (Figure 2b). Similar to the trend for total flower number, there was hardly any evident difference between the three groups with soil moisture of 50% or greater. However, an obvious reduction of yield was observed when the water content reduced to 40%, and even more severe losses for the 25-30% and 30-35% of soil moisture conditions with less than 1/5 of the control for the extreme drought. Furthermore, different from those under moderate or slight drought conditions (45-50% or more; Figure 2c-2e), plants with less water stopped producing siliques for a few days, longer under more severe drought (Figure 2f-2h), consistent with the lack of new flowers on those plants, as described above. We also noticed that some of the plants under extreme drought did not survive till the end.
Overview of transcriptome analyses of inflorescences under moderate drought condition
For each condition, we had at least two biological replicates for each time point and all the results were highly reproducible (all Pearson correlation coefficients > 0.98; Additional file 1). To focus on the genes significantly changed under drought compared with the well-watered condition, we only selected those whose expressions have: 1) more than two fold changes; 2) with q-values less than 0.01. According to these criteria, a total of 1830 genes were differentially expressed (up- and down-regulated) between the moderately drought at one or more of the four time points, Day 3, 4, 5 and 10 and the control group at C0 (Additional file 2). Specifically, 665 (M3/C0), 1049 (M4/C0), 1455 (M5/C0) and 659 (M10/C0) genes showed significantly differential expression at the respective time points (Additional file 3). Compared with C0, drought treated groups had increasing numbers of up-regulated genes during the early days of drought treatment, from 440 (at Day 3) up to 757 (at Day 4) and reaching the maximum at 1025 (at Day 5), but then decreased to 489 subsequently (at Day 10). A similar trend was found for the number genes that were significantly down-regulated under drought, increasing from 225 at Day 3 to 292 (Day 4) and 430 (Day 5), and then decreasing to 170 genes at day 10. Our results indicated that moderate drought induced altered expression of many genes in developing flowers, even though the morphology of these flowers seemed normal under such conditions.
Early responsive genes to moderate drought function in multiple stress responsive pathways
Comparison between genes responsive to moderate and severe drought
To compare putative gene functions between these clusters, we examined the GO categories for the four clusters above. In general, genes responsive to stimulus and pollen tube growth were enriched in all clusters, consistent with their expression changes under severe drought condition . In cluster I, gene functions in nucleosome assembly and response to GA and SA were enriched, suggesting that the observed decrease in stem elongation under moderate drought (Figure 1b) could be due to reduction of nucleosome assembly with possible effect on transcription, and that the reduced expression of genes for the GA signaling pathway was consistent with the fact that GA is important for stem elongation . The reduced number of SA signaling genes suggests that plants under moderate drought might be more susceptible to diseases. Genes in cluster II were enriched for functioning in pollen tube growth and response to water deprivation, suggesting that their elevated expression under both drought conditions were important and might be responsible for the nearly normal reproductive development under moderate drought. Regulatory genes including those controlling transcription, response to hormones including ABA, GA, JA, ET, SA, IAA, and water deprivation were enriched in the 3nd cluster, suggesting that more severe drought caused greater changes in the transcriptome in part by elevating the activities of transcriptional regulators and by strengthening hormone signaling. Interestingly, genes annotated with function in photosynthesis, pigment biosynthesis and response to red light were enriched in cluster IV, whose expression levels were higher under moderate drought condition than under severe drought condition. This suggests that the nearly normal development of these plants might have been facilitated by the enhanced functions of these genes.
Transcription factors showed induction in flowers specifically under moderate not severe drought condition
Dof-type zinc finger TF
C2H2-like zinc finger TF
Enrichment of known cis-elements in the regulatory regions of differentially expressed genes
Studies of stress responsive genes have identified cis-elements for transcriptional regulation, such as the ABRE, MYBR and DRE motifs [1, 22, 30–32]. To test whether such motifs might be associated with genes that were differentially expressed in response to moderate drought, we searched for the known motifs in the putative promoter sequence (1 kb upstream of start codon) of all 1830 differentially expressed genes (Additional file 8). We found 274 genes with the ABRE site (1639 with the core motif ACGT), 1220 with the MYB binding site (WAACCA), as well as 242 with the DRE motif (RCCGAC) in the putative promoter sequences. In addition to these known binding motifs potentially involved in drought response, we also searched for other known cis-acting regulatory elements for members of transcription factor families: NAC family (1378 with its core binding motif: CACG), MYC or the bHLH family (1776 with canonical E-box: CANNTG and 457 with core motif G-box: CATGTG) and WRKY (346 with its binding site: TGACY). Besides, several known consensuses involved in transcriptional activation were also identified in the putative sequences, such as TATA-box and CAAT-box. Because the MYB, MYC, NAC and WRKY transcription factor families also include members that have functions distinct from response to environmental stresses, the presence of these cis-elements alone does not imply regulation by stress signals. Nevertheless, the combination of stress-induced expression and presence of related cis-elements makes a stronger case for such regulation.
Genes for transcription factors were induced more by severe drought
We showed that the effect of drought on reproductive development was more drastic for severe drought than moderate drought. However, it is not known which genes are induced in a similar way, more under severe drought. By comparing the inflorescence transcriptome under severe and moderate drought conditions, we identified genes that were induced to a greater extent under severe drought, particularly in the 2nd cluster. From the GO results, we learned that transcription factors and transporters were among the enrich categories. We focused on the genes that have significantly more increased expression under severe drought compared with moderate drought, other than the genes that have preferential expression in moderate drought compared with well-watered condition (q < 0.01, two-fold change). At Day 3, no genes satisfying these criteria were found, but at later time points several genes with this expression pattern were identified (14 genes at Day 4, 62 genes at Day 5 and 26 genes at Day 10). This trend is consistent with our observation that the floral development resumed at Day 10 after a short pause following the initial drought treatment (Figure 1d).
Expression of genes known as transcription factors
Several transcription factor genes in this cluster are members of the NAC family, with 102 genes in Arabidopsis . Three NAC genes were induced by severe drought, including ANAC92, which belongs to the NAM clade. ANAC92 is known to function in the formation and development of the shoot apical meristem (SAM), and is redundant with CUC1 . Another study suggested that ANAC92 regulates senescence in response to salt by controlling several downstream genes in a stage dependent way , similar to what we have observed in this drought study. The other two NAC members are ANAC19 and ANAC47, both members of the AtNAC3 group. Previous studies support roles of NAC proteins in stress response in Arabidopsis and rice [11, 25].
Other transcription factors in this cluster included HSF1, PLATZ, OZF1 and OZF2. The OZFs are the closely related with two CCCH motifs . Both OZF factors are ABA-responsive and OZF2 is involved in the ABI2-mediated signaling pathway [39, 40]. It is possible that the two OZF function redundantly to assist the plant in response to various stresses. HSF1 is involved in response to a combination of drought and heat stress but more thorough experimental confirmation is needed .
Moderate drought induced genes for transport, ABA-dependent pathway and reproduction
Expression of genes involved in transportation
Amino acid transporter
Zinc ion binding
Expression of genes involved in embryogenesis and reproductive development
DUO1-activated ATPase 1
Seed storage 2S
Expression of genes involved in known stress responsive genes
Exordium like 2
PP2C GENE 1
PP2C GENE 2
Salt induced serine rich
Genes activated by moderate drought but not by severe drought
Signal pathways in response to moderate drought and severe drought
As mentioned above, 5284 genes were identified as differentially expressed under the SD condition and only 1830 genes under the MD condition. Among those genes, 1553 genes were detected in both studies. Using AgriGO software, we found different GO categories were enriched, including transcription regulator, transporter, enzyme and catalytic activity. The enrichment of similar categories was also observed in the group only differentially expressed under SD condition compared with control, except for the GO category of “binding activity” (Figure 4). This result indicated that the mechanisms plant employ to cope with varying levels of dehydration might be very similar.
85 transcription factors were differentially expressed under both MD and SD conditions, including members of DREB, NAC, AP2/ERF, MYB, bZIP, PLATZ, homeodomain, WRKY, zinc finger and HSF gene families. In addition to gene families mentioned above, genes in the AGL and BEH families were also identified in this category. The AGL family is commonly involved in the floral developmental process, thus it is consistent with our observation that only severe drought but not moderate drought, significantly influences the essential developmental process and cause loss of yield.
To find putative transcriptional regulatory network in response to drought, we investigated the putative promoter sequences of genes differentially expressed under drought condition. We searched for more than one hundred known binding motifs (from PLANTCARE) in the four clusters. Interestingly, the ABRE and ABRE-like binding motif were enriched in the 2nd and 3rd clusters (both within the first 0.5 kb and 1 kb). It is not surprising that ABA-independent pathway is very important in both moderate and severe drought response. Other binding motifs, such as E-box and G-box, were also enriched in these two clusters, suggesting putative transcription factors, such as those in the bHLH family, controlling some genes in the two clusters. The enrichment of cis-regulatory elements is not as significant when we searched in longer sequence (3 kb upstream of genes in each cluster). Though the NF-Y family members were enriched in the 2nd cluster, the binding site of NF-Y was not obviously enriched in any clusters using different length of putative promoter sequence. However, we still find many genes in this cluster with the CCAAT motif.
Inflorescence development is one of the essential constraint factors affecting plant yield. In this study, a moderate drought condition was applied to examine the inflorescence transcriptome to identify the gene activities that plant uses in response to drought, in a way similar to the recent study about the transcriptome analyses on inflorescence under severe drought condition . Although the effects of drought on reproductive development cannot fully be understood at this time and even vegetative organs may also play vital roles in success or failure to seed generation, the comparison of transcriptomes under two different water deficit conditions still can provide us a better understanding of not only the regulatory network in response to drought stress in flowers but also the different strategies that plants use to acclimate to different drought severities.
Reproductive acclimation to different drought conditions
Under moderate drought condition, Arabidopsis was able to achieve normal seed production on the main stem, similar to plants under well-watered condition, though there might be difference in seed contents and germination ability. The normal reproductive capacity of the main inflorescence indicates that the plant can maximize the use of limited water resources to ensure the production of the next generation even in an unfavorable environment. Similar observation was made in the study of Allocasuarina luehmannii whose vegetative growth appear to be normal under moderate drought, but not severe drought . In Geranium, moderate drought did not affect the overall quality of plants, but severe drought caused a reduction in the number of flowers per plant .
The sterile siliques found on the main stem of the plant grown under moderately severe, severe, and extreme drought conditions might be an important strategy for the plant to survive more extreme unfavorable environment. Under such extreme conditions, the sacrifice of a portion of the reproductive structures would limit the use of energy and water, allowing the precious resources to support the remaining reproduction for survival to the next generation. It is possible that alterations in the distribution of nitrogen and carbon assimilation to different plant parts to maintain reproductive ability are part of the response to drought, as reported before [52, 53].
Transcriptional reprogramming of inflorescence under moderate drought
Although the moderate drought did not cause dramatic morphological changes during reproductive development, a large number of genes (1830) were differentially expressed compared with those in well-watered plant. This was likely due to mechanisms that have evolved to protect plants against biotic and abiotic stresses without severe morphological changes, particularly to help plants to respond to mild environmental changes. Among these are the genes that function in response to stimulus especially ABA signaling and water deprivation and the genes that function in pollen tube growth, suggesting that these two aspects of drought response are critically important for plant growth under moderate drought conditions. One is accelerating the pollination and fertilization processes by activating those genes involving in pollen tube elongation; another aspect is promoting and strengthening the defense system to help plant to be more tolerant against drought stress. Therefore, it is likely that the reprogramming of the inflorescence transcriptome is at least in part important for the successful reproduction under moderate drought.
Difference of transcriptomes in response to moderate drought and severe drought
Transcriptomic analyses indicated that both moderate and severe drought conditions induced dramatic responses during flower development. Nuclear factor Y (NF-Y) is composed of three distinct subunits (NF-YA, NF-YB, and NF-YC). Interestingly, majority of genes encoding NF-Ys were found induced more under severe drought than moderate drought. However, seven out of the ten genes of the NF-YA subfamily were found to be induced by moderate drought but that is not true under severe drought condition, suggesting their possible roles in early response to drought stress and low intensity of drought. For example, NF-YA 2, 6, 8 and 10 were hardly induced at all under severe drought, indicating their specific roles in moderate drought response. NF-YA 3, 5 and 9 could be induced 3 days after moderate drought treatment, however , under severe drought they were induced much later (after day 5) (Figure 6). NF-YB 2 and NF-YB 3 are known as flowering time regulators and can interact with the floral promoting protein CONSTANS (CO) in the photoperiod dependent flowering regulatory network, and NF-YBs were also reported to interact with MADS-box genes in rice using an in vitro assay [24, 54]. NF-YA 5 and NF-YB 1 were reported to function in promoting drought resistance in Arabidopsis [26, 55]. NF-YB 6 and NF-YB 9 control early embryogenesis and embryo development, and also involved in seed maturation in Arabidopsis [49, 56]. In soybeans (Glycine max L.) GmNFYA3 is a positive regulator in drought response . Additional experiments of NF-YAs in Arabidopsis suggested their roles in modulating gene regulation through positive and negative mechanisms . Among the differentially expressed genes only due to moderate drought, we also identified that SOC1/AGL20 were significantly up-regulated by moderate drought. This could be caused by induction of NF-Ys and also indicate that SOC1 could act as an important node that connects both reproductive development and stress response.
Comparison with transcriptomes of vegetative tissues
To learn possible similarities and differences in gene activities affected by drought between reproductive and other tissues, we compared our results with other transcriptomes from vegetative tissues. Harb et al. studied transcriptome at vegetative stages in early response to soil drought condition in Arabidopsis  and found 2039 genes differentially expressed in response to moderate drought (30% soil capacity in Harb’s study) that is similar with 50% soil moisture in our study (Additional file 9). Among the 2039 genes, 372 were also differentially expressed in our data (1830 differentially expressed genes) (Additional file 10), including NF-Y2, NF-Y3, NF-Y5, NF-Y8 and NF-Y10, indicating that the NF-Y genes are important for response to moderate drought in both vegetative and reproductive organs in Arabidopsis. Among the 1458 genes that were differentially expressed only in our reproductive transcriptome but not in the Harb et al. study, the genes involved in response to stimulus such as ABA, GA, water deprivation and ROS are highly enriched (Additional file 9), suggesting that there might also be different regulatory pathway or genes functions in different tissue types in response to drought stress. Further efforts are needed to elucidate the mechanistic differences in response in different tissue types and to different drought severities.
In conclusion, we observed that moderate drought did not cause dramatic reduction of reproductive yield, but did induce altered expression of many genes, although fewer than those under severe drought. A comparison of transcriptomes in response to moderate or severe drought, we discovered that the CCAAT-binding factors/NF-Ys were specifically induced by moderate drought and might have a specific function under this condition. Our results indicate that plants respond to mild water stress by inducing many genes, whose function are likely important in protecting plants against the stresses and in ensuring reproductive success under such conditions.
In this study, morphological analyses under different water conditions were performed on Col-0, which has been sequenced completely. Drought assay was done as described in our previous study with some minor changes . Seeds were directly planted into pots containing 100 g soil consisting of dry soil (Metro-Mix 360, Sun Gro Horticulture Canada Ltd) and greens grade (Turface profile greens grade, Profile Products LLC) by a ratio 3:2 in volume. The water-holding capacity of 90 g (defined as 90% soil moisture, also indicated as 90% field capacity) as Well-watered condition was measure by weighing on a scale. 70g, 50g, 40g, 35g and 30 g of water, respectively, were added to the soil mixture to achieve different water-deficit conditions. After two days of seed stratification in dark at 4°C, all the plants were grown in growth chamber under normal growth condition (22°C, 16 h/8 h, day/night photoperiod, ~300 μmol m-2 s-1 photon flux, 60% humidity) until the plant had just begun to flower (bolting was visible with a main inflorescence stem of about 1 cm and unopened floral buds) when plants were subjected to different types of drought treatment when the main stem is about 1 cm high . Plants for morphological analyses were then observed until almost all the siliques were matured and ready to be harvested (about 50 days after planting).
Samples collected for microarray were prepared as follow: the moderate drought (MD) and severe drought (SD) treatments started by withholding water. The relative soil moisture content reduced to the expected degree (MD: 50% and SD: 35%) three days after the starting point (C0). We maintained the soil water condition (30% - 35%, 45% - 50%, and 85% - 90% in control group) for 3, 4, 5 and 10 days (labeled as D 3, D 4, D 5 and D 10, started from water withholding day). Unopened flower samples were then collected, from both M and S drought treated groups and control groups. Two biological replicates from the inflorescences were collected at each time point from each group.
The condition of our drought assay was important to obtain reproducible results; different soil conditions or chemical treatments that mimic osmotic stress could result in different transcriptome changes.
Following the Affymetrix GeneChip Expression Analysis Overview described on the website (http://www.affymetrix.com), cRNAas were synthesized for hybridization as described . Hybridization, washing, staining, scanning and data collection were performed in Genomics Core Facility at Pennsylvania State University.
Normalization was applied using Bioconductor package in R by RMA, and all the expression values were converted to logarithms base 2. We then used LIMMA package to compare signals from control and well-watered inflorescences. Only genes with more than two-fold changes were selected in addition to the statistical criterion: Q-value (FDR) less than 0.01.
K-means clustering of co-expressed genes was performed by MeV 4.9 . The normalized values of hybridization signal in log2 were used in K-means analysis, and the heatmap was generated base on the difference from the mean of the values of each gene. For the identification of the functions of the differentially expressed genes, the annotations of genes on ATH1 microarray chip were downloaded from Affymetrix website and we used the GO categorization function on TAIR website. To verify whether one category is enriched compared with the whole genome, we applied hypergeometric test and only the categories with p-value less than 0.05 were called statistically enriched group.
cis-regulatory element analysis and GO analysis
Possible promoter sequences of all genes on the microarray chip (1 kb upstream of the start codon) were obtained from TAIR website. The numbers of binding sites of different transcriptional regulators were then counted. The identification of cis-regulatory binding site was conducted by perl . The binding motifs were obtained from Gene Regulation and PlantCARE . The Gene Ontology (GO) analysis was done by the agriGO software . Significance bar represents p-value from 1 × 10-1 to 1 × 10-10.
Availability of supporting data
The raw data sets supporting the results of this article are available in the Gene Expression Omnibus (GEO) repository under accession No GSE55431 (http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE55431). The data and analyses of transcriptomes under serve drought are available in GEO with accession No GSE40998 (http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE40998) .
We greatly appreciate the help of Dr. Craig Praul in performing microarray hybridizations. We also thank Ms. Yi Hu for plant care and lab management. We thank the suggestions and comments from Drs. Xiaofan Zhou, Xinwei Han and Yazhou Sun on microarray data analyses. This work was supported by a US Department of Energy grant to H.M. and funds from Department Biology and the Huck Institutes of the Life Sciences, the Pennsylvania State University, and Fudan University.
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