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9.10: Flowering Plants - Biology

9.10: Flowering Plants - Biology



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So what exactly is a flower?

This closeup view of a lily flower shows the fine detail of this structure. Why are flowers so colorful? What is the purpose of all the parts? They were one of the last adaptations of the plant kingdom, suggesting immense evolutionary significance.

Flowering Plants

Angiosperms, or flowering seed plants, form seeds in ovaries. As the seeds develop, the ovaries may develop into fruits. Flowers attract pollinators, and fruits encourage animals to disperse the seeds.

Parts of a Flower

A flower consists of male and female reproductive structures. The main parts of a flower are shown in Figure below. They include the stamen, pistil, petals, and sepals.

  • The stamen is the male reproductive structure of a flower. It consists of a stalk-like filament that ends in an anther. The anther contains pollen sacs, in which meiosis occurs and pollen grains form. The filament raises the anther up high so its pollen will be more likely to blow in the wind or be picked up by an animal pollinator.
  • The pistil is the female reproductive structure of a flower. It consists of a stigma, style, andovary. The stigma is raised and sticky to help it catch pollen. The style supports the stigma and connects it to the ovary, which contains the egg. Petals attract pollinators to the flower. Petals are often brightly colored so pollinators will notice them.
  • Sepals protect the developing flower while it is still a bud. Sepals are usually green, which camouflages the bud from possible consumers.

A flower includes both male and female reproductive structures.

Flowers and Pollinators

Many flowers have bright colors, strong scents, and sweet nectar to attract animal pollinators. They may attract insects, birds, mammals, and even reptiles. While visiting a flower, a pollinator picks up pollen from the anthers. When the pollinator visits the next flower, some of the pollen brushes off on the stigma. This allows cross-pollination, which increases genetic diversity.

Other Characteristics of Flowering Plants

Although flowers and their components are the major innovations of angiosperms, they are not the only ones. Angiosperms also have more efficient vascular tissues. Additionally, in many flowering plants the ovaries ripen into fruits. Fruits are often brightly colored, so animals are likely to see and eat them and disperse their seeds (see Figure below).

Brightly colored fruits attract animals that may disperse their seeds. It’s hard to miss the bright red apples on these trees.

Evolution of Flowering Plants

Flowering plants are thought to have evolved at least 200 million years ago from gymnosperms like Gnetae. The earliest known fossils of flowering plants are about 125 million years old. The fossil flowers have male and female reproductive organs but no petals or sepals.

Scientists think that the earliest flowers attracted insects and other animals, which spread pollen from flower to flower. This greatly increased the efficiency of fertilization over wind-spread pollen, which might or might not actually land on another flower. To take better advantage of this “animal labor,” plants evolved traits such as brightly colored petals to attract pollinators. In exchange for pollination, flowers gave the pollinators nectar.

Giving free nectar to any animal that happened to come along was not an efficient use of resources. Much of the pollen might be carried to flowers of different species and therefore wasted. As a result, many plants evolved ways to “hide” their nectar from all but very specific pollinators, which would be more likely to visit only flowers of the same species. For their part, animal pollinators co-evolved traits that allowed them to get to the hidden nectar. Two examples of this type of co-evolution are shown in Figure below.

The hummingbird has a long narrow bill to reach nectar at the bottom of the tube-shaped flowers. The bat is active at night, so bright white, night-blooming flowers attract it. In each case, the flowering plant and its pollinator co-evolved to become better suited for their roles in the symbiotic relationship.

Some of the most recent angiosperms to evolve are grasses. Humans started domesticating grasses such as wheat about 10,000 years ago. Why grasses? They have many large, edible seeds that contain a lot of nutritious stored food. They are also relatively easy to harvest. Since then, humans have helped shaped the evolution of grasses, as illustrated by the example in Figure below. Grasses supply most of the food consumed by people worldwide. What other grass seeds do you eat?

The plant on the left, called teosinte, is the ancestor of modern, domesticated corn, shown on the right. An intermediate stage is pictured in the middle. How were humans able to change the plant so dramatically?

Classification of Flowering Plants

There are more than a quarter million species of flowering plants, and they show tremendous diversity. Nonetheless, almost all flowering plants fall into one of three major groups: monocots, eudicots, or magnolids. The three groups differ in several ways. For example, monocot embryos form just one cotyledon, whereas eudicot and magnolid embryos form two cotyledons. The arrangement of their vascular tissues is also different. Examples of the three groups of flowering plants are given in Table below.

GroupSample FamiliesSample Families
Monocots

Grasses

Orchids

Eudicots

Daisies

Peas

Magnolids

Magnolias

Avocados

Summary

  • Most modern seed plants are angiosperms that produce seeds in the ovaries of flowers.
  • Ovaries may develop into fruits.
  • Flowers attract pollinators and fruits are eaten by animals. Both traits aid the dispersal of seeds.

Review

  1. Describe the male and female reproductive structures of flowers.
  2. State how fruits help flowering plants reproduce.
  3. Explain how flowering plants and their animal pollinators co-evolved.
  4. Define monocot.

Boraginaceae

The APG IV system from 2016 classifies the Boraginaceae as single family of the order Boraginales within the asterids. [4] Under the older Cronquist system it was included in Lamiales, but it is now clear that it is no more similar to the other families in this order than they are to families in several other asterid orders. A revision of the Boraginales, also from 2016, split the Boraginaceae in eleven distinct families: [5] Boraginaceae sensu stricto, Codonaceae, Coldeniaceae, Cordiaceae, Ehretiaceae, Heliotropiaceae, Hoplestigmataceae, Hydrophyllaceae, Lennoaceae, Namaceae, and Wellstediaceae.

These plants have alternately arranged leaves, or a combination of alternate and opposite leaves. The leaf blades usually have a narrow shape many are linear or lance-shaped. They are smooth-edged or toothed, and some have petioles. Most species have bisexual flowers, but some taxa are dioecious. Most pollination is by hymenopterans, such as bees. Most species have inflorescences that have a coiling shape, at least when new, called scorpioid cymes. [6] The flower has a usually five-lobed calyx. The corolla varies in shape from rotate to bell-shaped to tubular, but it generally has five lobes. It can be green, white, yellow, orange, pink, purple, or blue. There are five stamens and one style with one or two stigmas. The fruit is a drupe, sometimes fleshy. [7]

Most members of this family have hairy leaves. The coarse character of the hairs is due to cystoliths of silicon dioxide and calcium carbonate. These hairs can induce an adverse skin reaction, including itching and rash in some individuals, particularly among people who handle the plants regularly, such as gardeners. In some species, anthocyanins cause the flowers to change color from red to blue with age. This may be a signal to pollinators that a flower is old and depleted of pollen and nectar. [8]


A Universal Probe Set for Targeted Sequencing of 353 Nuclear Genes from Any Flowering Plant Designed Using k-Medoids Clustering

Sequencing of target-enriched libraries is an efficient and cost-effective method for obtaining DNA sequence data from hundreds of nuclear loci for phylogeny reconstruction. Much of the cost of developing targeted sequencing approaches is associated with the generation of preliminary data needed for the identification of orthologous loci for probe design. In plants, identifying orthologous loci has proven difficult due to a large number of whole-genome duplication events, especially in the angiosperms (flowering plants). We used multiple sequence alignments from over 600 angiosperms for 353 putatively single-copy protein-coding genes identified by the One Thousand Plant Transcriptomes Initiative to design a set of targeted sequencing probes for phylogenetic studies of any angiosperm group. To maximize the phylogenetic potential of the probes, while minimizing the cost of production, we introduce a k-medoids clustering approach to identify the minimum number of sequences necessary to represent each coding sequence in the final probe set. Using this method, 5-15 representative sequences were selected per orthologous locus, representing the sequence diversity of angiosperms more efficiently than if probes were designed using available sequenced genomes alone. To test our approximately 80,000 probes, we hybridized libraries from 42 species spanning all higher-order groups of angiosperms, with a focus on taxa not present in the sequence alignments used to design the probes. Out of a possible 353 coding sequences, we recovered an average of 283 per species and at least 100 in all species. Differences among taxa in sequence recovery could not be explained by relatedness to the representative taxa selected for probe design, suggesting that there is no phylogenetic bias in the probe set. Our probe set, which targeted 260 kbp of coding sequence, achieved a median recovery of 137 kbp per taxon in coding regions, a maximum recovery of 250 kbp, and an additional median of 212 kbp per taxon in flanking non-coding regions across all species. These results suggest that the Angiosperms353 probe set described here is effective for any group of flowering plants and would be useful for phylogenetic studies from the species level to higher-order groups, including the entire angiosperm clade itself.

Keywords: Angiosperms Hyb-Seq k-means clustering k-medoids clustering machine learning nuclear genes phylogenomics sequence capture target enrichment.

© The Author(s) 2018. Published by Oxford University Press on behalf of the Society of Systematic Biologists.

Figures

Overview of probe design and…

Overview of probe design and phylogenetic considerations. Given a hypothetical gene ABCD1 ,…

Comparison between the k-medoids method…

Comparison between the k-medoids method of selecting representative sequences with using the closest…

Heatmap of gene recovery efficiency.…

Heatmap of gene recovery efficiency. Each row is one sample, and each column…

Relationship between reads mapping to…

Relationship between reads mapping to the target genes and the number of loci…

Total length of sequence recovery…

Total length of sequence recovery for both coding and non-coding regions across 353…


Results

Idd8-3 and AKIN10-overexpresser exhibit delayed flowering under long days

As an initial step to investigate the functional relationship between AKIN10 and IDD8 in flowering time control, we compared the flowering phenotypes of Arabidopsis plants that have altered expression of IDD8 and AKIN10 genes. T-DNA insertional mutants of AKIN10 and AKIN11 genes (akin10-1 and akin11-1, respectively) were obtained from the Arabidopsis Biological Resource Center (ABRC, Ohio state university, OH). Gene expression analysis revealed that they are loss-of-function mutants (Additional file 1). We also produced transgenic plants overexpressing either AKIN10 or AKIN11 gene under the control of the cauliflower mosaic virus (CaMV) 35S promoter, resulting in 10-ox or 11-ox, respectively (Additional file 2). We similarly produced transgenic plants overexpressing IDD8, resulting in 8-ox.

We examined the flowering phenotypes of the plants grown under long days (LDs, 16-h light and 8-h dark) by counting the numbers of rosette leaves at bolting and the days to bolting. The 8-ox plants and the akin10-1 and akin11-1 mutants did not exhibit any discernible flowering phenotypes under our assay conditions (Figures 1A and 1B). In contrast, the 10-ox and 11-ox plants exhibited delayed flowering, as observed in idd8-3 mutant. The delay of flowering time was more prominent in 10-ox than in 11-ox (Figure 1B). The similar flowering phenotypes raised a possibility that loss of IDD8 function is related with overproduction of AKIN10 and AKIN11 in regulating flowering time. In support of this hypothesis, the expression of SUS4 and SUC genes was suppressed in the 10-ox plants but up-regulated in the akin10-1 mutant (Additional file 3), as observed in the idd8-3 mutant and the 8-ox plants, respectively [20].

AKIN10 overexpression delays flowering. Plants were grown in soil under LDs for 6 weeks before taking photographs (A). Flowering times were measured by counting the days to bolting and rosette leaf numbers at bolting (B, left and right panels, respectively). Transgenic plants overexpressing IDD8 (8-ox1 and 8-ox2), AKIN10 (10-ox), and AKIN11 (11-ox) and their gene knockout mutants were analyzed. The countings of approximately 20 plants were averaged and statistically analyzed using Student t-test (*P < 0.01, difference from col-0). Bars indicate standard error of the mean.

IDD8 interacts with AKIN10 in the nucleus

On the basis of the similar flowering phenotypes of idd8-3 mutant and AKIN-overexpressing plants and the biochemical nature of IDD8 transcription factor and SnRK1 kinases, we hypothesized that IDD8 interacts with the SnRK1 kinases.

Yeast two-hybrid assays did not show any positive interactions between IDD8 and AKIN10 (data not shown). We therefore employed in vitro pull-down assays using recombinant glutathione S-transferase-AKIN10 (GST-AKIN10) and GST-AKIN11 fusion proteins, which were produced in E.coli cells, and 35 S-labelled IDD8 polypeptides produced by in vitro translation. While IDD8 did not interact with GST alone, it strongly interacted with GST fusions of AKIN10 and AKIN11 (Figure 2A). The lack of IDD8-AKIN interactions in yeast cells might be due to an intrinsic property of AKIN proteins, as has been observed previously [27,30].

IDD8 interacts with AKIN proteins in the nucleus. A in vitro pull-down assay. Recombinant GST-AKIN10 and GST-AKIN11 fusion proteins produced in E. coli cells and in vitro translated, radio-labelled IDD8 polypeptides were used (upper panel). Recombinant GST was used as negative control. The ‘Input’ represents 20% of the labeling reaction. Part of Coomassie Blue-stained gel was displayed as a loading control (lower panel). kDa, kilodalton. B BiFC assay. nYFP-IDD8 and cYFP-AKIN fusions and cyan fluorescent protein (CFP)-ICE1 fusion, which was used as a nuclear marker, were coexpressed transiently in Arabidopsis protoplasts. IDD8-AKIN interactions were visualized by differential interference contrast (DIC) and fluorescence microscopy. Scale bars, 10 μm.

We also performed bimolecular fluorescence complementation (BiFC) assays to examine whether the IDD8-AKIN interactions occur in plant cells. Coexpression of the N-terminal half of yellow fluorescent protein (YFP) fused to IDD8 (nYFP-IDD8) and the C-terminal half of YFP fused to AKIN10 (cYFP-AKIN10) or AKIN11 (cYFP-AKIN11) in Arabidopsis protoplasts revealed that the IDD8-AKIN interactions occur in the nucleus (Figure 2B, Additional file 4), indicating that IDD8 interacts with AKIN proteins in planta.

AKIN10 phosphorylates IDD8

AKIN10 and AKIN11 are the catalytic subunits of SnRK1 kinases [24,27]. Protein phosphorylation is one of the primary biochemical mechanisms that modulate the activities of transcription factors in plants [26,31,32]. We therefore examined whether AKIN proteins phosphorylate IDD8.

We produced recombinant maltose-binding protein-IDD8 (MBP-IDD8) and GST-AKIN fusion proteins in E.coli cells, which were purified by affinity chromatography and immunologically quantified (Additional file 5A). The in vitro kinase assays showed that AKIN10 possesses an autophosphorylation activity, while AKIN11 does not (Figure 3). It was also evident that AKIN10, but not AKIN11, phosphorylates IDD8. Although both 10-ox and 11-ox plants exhibited delayed flowering (Figure 1) and IDD8 interacts with both AKIN10 and AKIN11, IDD8 may not be directly targeted by AKIN11 at least in controlling flowering time.

Phosphorylation of IDD8 by AKIN10. The in vitro phosphorylation assays were conducted using recombinant GST-AKIN10 and GST-AKIN11 fusion proteins and MBP-IDD8 fusion protein prepared in E. coli cells (upper panel). Part of Coomassie Blue-stained gel was displayed as a loading control (lower panel). kDa, kilodalton.

To identify the Ser and Thr residues of IDD8 targeted by AKIN10, we searched for putative target residues using the NetPhos2 algorithm (http://www.cbs.dtu.dk/services/NetPhos/). The computer-assisted analysis identified 18 Ser and 5 Thr residues that were predicted to be phosphorylated by SnRK1. Among the 23 residues, only the sequence contexts around Thr-98, Ser-178, and Ser-182 partially matched to the consensus sequence established for SnRK1 kinases [26] (Additional file 6). The three residues were mutated to alanine, resulting in T98A, S178A, and S182A (Figure 4A), and the mutated IDD8 proteins were prepared as MBP fusions in E. coli cells and immunologically quantified (Additional file 5B). The recombinant MBP-IDD8 proteins were then subjected to in vitro phosphorylation assays. It was found that the phosphorylation of S182A was significantly reduced by more than 90% compared to that of wild-type IDD8 protein (Figure 4B). In contrast, T98A and S178A were still phosphorylated with a reduction of approximately 50%. Liquid chromatography-tandem mass spectrometry (LC-MS/MS) also supported the notion that S182 is a major site for AKIN10-mediated phosphorylation (Additional file 7).

Identification of phosphorylation residues in IDD8. A Predicted phosphorylation residues in IDD8. Potential phosphorylation residues were predicted using the NetPhos-based analysis tool (http://www.cbs.dtu.dk/services/NetPhos/). The predicted serine (S) and threonine (T) residues were mutated to alanine (A). ZF, zinc finger. aa, amino acid. B in vitro phosphorylation assay. The assays were conducted using recombinant GST-AKIN10 and MBP-IDD8 fusion proteins prepared in E. coli cells (upper panel). Part of Coomassie Blue-stained gel was displayed as a loading control (middle panel). Black arrowheads indicate IDD8 protein. White arrowheads indicate AKIN10 protein. kDa, kilodalton. The relative intensities of the phosphorylation bands were calculated in comparison to those on Coomassie Blue-stained gel (lower panel). Experimental triplicates were averaged and statistically analyzed using Student t-test (*P < 0.01, **P < 0.05, difference from wild-type IDD8). Bars indicate standard error of the mean.

AKIN10 does not affect the subcellular localization of IDD8

Protein phosphorylation influences diverse structural and functional aspects of transcription factors, such as protein stability, subcellular localization, and transcriptional activation activity [26,32,33]. It has been reported that AKIN10 regulates the protein stability of the B3-domain-containing transcription factor FUSCA3 (FUS3) during lateral organ development and floral transition [26]. Therefore, a question was how AKIN10-mediated phosphorylation regulates IDD8 function in flowering time control.

We first examined whether protein phosphorylation affects the stability of IDD8 protein using transgenic plants overexpressing IDD8-MYC fusion driven by the CaMV 35S promoter in either Col-0 plant or akin10-1 mutant. The transgenic plants were incubated either in constant light or in complete darkness for 2 days. They were also incubated in the presence of 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU), which is a specific inhibitor of photosynthesis [24], in constant light. IDD8 proteins were then immunologically detected using an anti-MYC antibody. The results showed that in the Col-0 background, the IDD8 levels were reduced in darkness, and the reduction was more prominent in the presence of DCMU (Additional file 8A, upper panel), which is probably due to dark-induced degradation of IDD8 protein. Alternatively, the reduction would be at least in part attributable to the transcriptional suppression of IDD8 gene by low sugar levels. Notably, the patterns of IDD8 abundance were similarly observed in akin10-1 background, although the overall levels were lower than those in Col-0 background. Quantitative real-time RT-PCR (qRT-PCR) showed that the levels of IDD8 transcripts were lower in akin10-1 background (Additional file 8A, lower left panel). However, the levels of IDD8 protein relative to those of IDD8 transcripts were similar in Col-0 and akin10-1 backgrounds (Additional file 8A, lower right panel). Together, these observations indicate that AKIN10 does not affect the stability of IDD8 protein.

We next examined whether AKIN10-mediated phosphorylation influences the subcellular localization of IDD8 by transient expression of a green fluorescent protein (GFP)-IDD8 fusion in Arabidopsis protoplasts prepared from Col-0, akin10-1, and 10-ox plants and using transgenic plants overexpressing a GFP-IDD8 fusion in Col-0 and 10-ox backgrounds. The roots of the transgenic plants were visualized by fluorescence microscopy. GFP signals were detected predominantly in the nuclei of root cells of both Col-0 and 10-ox backgrounds (Additional files 8B and C), indicating that the subcellular distribution of IDD8 is not affected by AKIN10-mediated protein phosphorylation.

AKIN10 inhibits the transcriptional activation activity of IDD8

IDD8 binds directly to SUS4 gene promoter containing the conserved CTTTTGTCC motif [20]. We therefore asked whether AKIN10 affects the DNA-binding property of IDD8. We performed chromatin immunoprecipitation (ChIP) assays using 35S:MYC-IDD8 and 35:MYC-IDD8 akin10-1 plants. IDD8-binding sequence (BS) and non-binding sequence (nBS) within the SUS4 gene promoter were included in the assays (Additional file 9A). The assays revealed that IDD8 does not bind to nBS sequence (Additional file 9B). In contrast, IDD8 efficiently bound to BS sequence. Notably, IDD8 also bound efficiently to BS sequence in akin10-1 background, indicating that AKIN10 does not affect the DNA-binding property of IDD8.

A remaining question was whether AKIN10 affects the transcriptional activation activity of IDD8. To address this question, we performed transient β-galactosidase (GUS) expression assays by coexpressing a series of reporter and effecter vectors in Arabidopsis protoplasts (Figure 5A). Notably, AKIN10 reduced the transcriptional activation activity of IDD8 by approximately 65% (Figure 5B). In contrast, AKIN11 reduced the IDD8 activity only slightly, further supporting the notion that AKIN11 is not directly related with IDD8.

AKIN10 inhibits IDD8 transcription factor activity. A Reporter and effector vector constructs. A full-size IDD8 cDNA was fused in-frame to the 3′ end of GAL4 DNA-binding domain (DB)-coding sequence in the effector vector. B SnRK1-mediated inhibition of IDD8 transcriptional activation activity. GAL4 transient expression assays were performed using Arabidopsis protoplasts, as described previously [20]. The Renilla luciferase gene was used as an internal control to normalize the values in individual assays. ARF5M is a transcriptional activator control. ARF1M is a transcriptional repressor control. Three measurements of GUS activity were averaged and statistically analyzed using Student t-test (*P < 0.01, difference from IDD8). Bars indicate standard error of the mean. C Transcription factor activity of mutated IDD8. The mutated IDD8 (mIDD8) harbors S178A and S182A substitutions. GUS activity measurements were performed as described in (B). Bars indicate standard error of the mean (t-test, *P < 0.01, difference from IDD8). D Effects of sugar deprivation on IDD8 transcription factor activity. The GUS reporter and the IDD8 effector vectors were cotransformed into Arabidopsis protoplasts that were prepared from either Col-0 plant or akin10-1 mutant (left and right panels, respectively). The Arabidopsis protoplasts were then treated with 20 μM DCMU for 6 h before GUS activity measurements. Three measurements were averaged and statistically analyzed (t-test, *P < 0.01, difference from mock). Bars indicate standard error of the mean.

The transient GUS expression assays also showed that a mutated IDD8 protein (mIDD8) harboring the S178A and S182A substitutions is transcriptionally active comparable to the wild-type IDD8 protein (Figure 5C). It was notable that whereas AKIN10 reduced the IDD8 activity, it did not affect the mIDD8 activity, indicating that IDD8 phosphorylation by AKIN10 is important for the suppression of the IDD8 activity.

It is known that AKIN10 is activated under low-sugar conditions [25]. We therefore examined the effects of sugar deprivation on IDD8 activity by transient GUS expression assays using Arabidopsis protoplasts prepared from Col-0 plants and akin10-1 mutant. Arabidopsis protoplasts were treated with DCMU to mimic sugar deprivation conditions before the assays. It was found that whereas DCMU detectably reduced the IDD8 activity in Col-0 plants, it did not affect the IDD8 activity in akin10-1 mutant (Figure 5D), demonstrating that AKIN10 suppresses IDD8 activity under sugar deprivation conditions.

AKIN10-mediated phosphorylation of IDD8 is relevant for flowering time control

Our data showed that AKIN10 phosphorylates IDD8 to reduce its transcriptional activation activity in response to sugar deprivation. We next examined whether the phosphorylation of IDD8 by sugar deprivation-activated AKIN10 is functionally relevant for flowering time control. We crossed idd8-3 with akin10-1, resulting in idd8-3 akin10-1 double mutant (Additional file 10). Flowering time measurements showed that the idd8-3 akin10-1 double mutant exhibited delayed flowering as observed in the idd8-3 mutant (Figure 6A). What was unexpected was that the delay of flowering was more severe in the double mutant, suggesting that AKIN10 might target additional flowering time modulators other than IDD8 (see below).

Flowering phenotypes and molecular characterization of idd8-3 akin10-1 double mutant. The idd8-3 mutant was crossed with the akin10-1 mutant, resulting in idd8-3 akin10-1 double mutant. A Flowering phenotypes. Plants were grown in soil under LDs for 6 weeks before taking photographs (left panel). Leaf numbers of 20 plants at bolting were averaged and statistically analyzed using the Student t-test (*P < 0.01, difference from Col-0) (right panel). Bars indicated standard error of the mean. B Expression of flowering time genes. Aerial parts of two-week-old plants grown in soil were harvested at zeitgeber time 16 for the extraction of total RNA. Transcript levels were examined by qRT-PCR. Biological triplicates were averaged and statistically analyzed using Student t-test (*P < 0.01, difference from Col-0). Bars indicate standard error of the mean.

qRT-PCR assays on flowering time genes showed that FT gene and its downstream targets SOC1 and APPETALA 1 (AP1) genes were suppressed in the single and double mutants (Figure 6B), consistent with their delay flowering phenotypes. Notably, the floral repressor FLC was significantly induced in the idd8-3 akin10-1 mutants, which might be related with the severity of delayed flowering in the double mutant (Figure 6A).

Altogether, our data demonstrate that SnRK1 inhibits the transcriptional activation activity of IDD8 transcription factor through protein phosphorylation to delay flowering under low-sugar conditions (Figure 7). This working scenario explains the suppression of IDD8 function under sugar deprivation conditions [20]. We propose that the SnRK1-IDD8 signaling module provides a molecular clue for the long-lasting interest in the metabolic control of flowering in plants.

Schematic model of AKIN10 function in flowering time control. Sugar deprivation conditions, which are encountered in early vegetative phase, activate AKIN10 that negatively regulates IDD8 transcription factor. During the reproductive phase transition, increased sugar availability deactivates AKIN10, resulting in flowering transition. It is also likely that AKIN10 negatively regulates FLC function either directly or indirectly via an unidentified regulator of FLC.


THE C2 OXIDATIVE PHOTOSYNTHETIC CARBON CYCLE

Abstract

▪ Abstract The C2 oxidative photosynthetic carbon cycle plus the C3 reductive photosynthetic carbon cycle coexist. Both are initiated by Rubisco, use about equal amounts of energy, must regenerate RuBP, and result in exchanges of CO2 and O2 to . Read More

Figure 1: The C2 and C3 cycles of photosynthetic carbon metabolism. This scheme (9, 10) emphasizes that the two cycles coexist, that both represent about equal parts of the process, that carboxylase .


A Bridge to the World

Zhi-Hong Xu is a plant physiologist who studied botany at Peking University (1959–1965). He joined the Shanghai Institute of Plant Physiology (SIPP), Chinese Academy of Sciences (CAS), as a graduate student in 1965. He recalls what has happened for the institute, during the Cultural Revolution, and he witnessed the spring of science eventually coming to China. Xu was a visiting scholar at the John Innes Institute and in the Department of Botany at Nottingham University in the United Kingdom (1979–1981). He became deputy director of SIPP in 1983 and director in 1991 he also chaired the State Key Laboratory of Plant Molecular Genetics SIPP (1988–1996). He worked as a visiting scientist in the Institute of Molecular and Cell Biology, National University of Singapore, for three months each year (1989–1992). He served as vice president of CAS (1992–2002) and as president of Peking University (1999–2008). Over these periods he was heavily involved in the design and implementation of major scientific projects in life sciences and agriculture in China. He is an academician of CAS and member of the Academy of Sciences for the Developing World. His scientific contributions mainly cover plant tissue culture, hormone mechanism in development, as well as plant developmental response to environment. Xu, as a scientist and leader who has made an impact in the community, called up a lot of excellent young scientists returning to China. His efforts have promoted the fast development of China's plant and agricultural sciences.


Question 1.
What is the function of filiform apparatus in an angiospermic embryo sac?
(a) Brings about opening of the pollen tube
(b) Guides the pollen tube into a synergid
(c) Prevents entry of more than one pollen tube into a synergid
(d) None of these
Answer:
(b) Guides the pollen tube into a synergid

Question 2.
The female gametophyte of a typical dicot at the time of fertilisation is
(a) 8 – celled
(b) 7 – celled
(c) 6 – celled
(d) 5 – celled
Answer:
(b) 7 – celled

Question 3.
Polygonum type of embryo sac is
(a) 8 – nucleate, 7 – celled
(b) 8 – nucleate, 8 – celled
(c) 7 – nucleate, 7 – celled
(d) 4 – nucleate, 3 – celled
Answer:
(a) 8 – nucleate, 7 – celled

Question 4.
Both chasmogamous and cleistogamous flowers are present in
(a) Helianthus
(b) Commelina
(c) Rosa
(d) Gossypium
Answer:
(b) Commelina

Question 5.
Even in absence of pollinating agents seed-setting is assured in
(a) Commelina
(b) Zostera
(c) Salvia
(d) Fig
Answer:
(a) Commelina

Question 6.
Male and female flowers are present on different plants (dioecious) to ensure xenogamy, in
(a) papaya
(b) bottle gourd
(c) maize
(d) all of these.
Answer:
(a) papaya

Question 7.
Feathery stigma occurs in
(a) pea
(b) wheat
(c) Datura
(d) Caesalpinia
Answer:
(b) wheat

Question 8.
Plants with ovaries having only one or a few ovules are generally pollinated by
(a) bees
(b) butterflies
(c) birds
(d) wind
Answer:
(d) wind

Question 9.
Which of the following is not a water pollinated plant ?
(a) Zostera
(b) Vallisneria
(c) Hydrilla
(d) Cannabis
Answer:
(d) Cannabis

Question 10.
Spiny or sticky pollen grains and large, attractively coloured flowers are associated with
(a) hydrophily
(b) entomophily
(c) ornithophily
(d) anemophily
Answer:
(b) entomophily

Question 11.
Endospermic seeds are found in
(a) castor
(b) barley
(c) coconut
(d) all of these
Answer:
(d) all of these

Question 12.
In albuminous seeds, food is stored in _______ and in non albuminous seeds, it is stored in _______.
(a) endosperm, cotyledons
(b) cotyledons, endosperm
(c) nucellus, cotyledons
(d) endosperm, radicle
Answer:
(a) endosperm, cotyledons

Question 13.
Persistent nucellus is called as _______ and is found in _______.
(a) perisperm, black pepper
(b) perisperm, groundnut ‘
(c) endosperm, black pepper
(d) endosperm groundnut
Answer:
(a) perisperm, black pepper

Question 14.
Indentify the wrong statement regarding post-fertilisation development.
(a) The ovary wall develops into pericarp.
(b) The outer integument of ovule develops into tegmen.
(c) The fusion nucleus (triple nucleus) develops into endosperm.
(d) The ovule develops into seed.
Answer:
(b) The outer integument of ovule develops into tegmen.

Question 15.
Polyembryony commonly occurs in
(a) banana
(b) tomato
(c) potato
(d) citrus.
Answer:
(d) citrus.

Question 16.
An embryo may sometimes develop from any cell of embryo sac other than egg. It is termed as
(a) apospory
(b) apogamy
(c) parthenogenesis
(d) parthenocarpy
Answer:
(b) apogamy

Question 17.
Embryo sac is to ovule as _______ is to an anther.
(a) Stamen
(b) filament
(c) pollen grain
(d) androecium
Answer:
(c) pollen grain

Question 18.
The outermost and innermost wall layers of microsporangium in an anther are respectively
(a) endothecium and tapetum
(b) epidermis and endodermis
(c) epidermis and middle layer
(d) epidermis and tapetum.
Answer:
(d) epidermis and tapetum.

Question 19.
During microsporogenesis, meiosis occurs in
(a) endothecium
(b) microspore mother cells
(c) microspore tetrads
(d) pollen grains
Answer:
(b) microspore mother cells

Question 20.
From among the sets of terms given below, identify those that are associated with the gynoecium.
(a) Stigma, ovule, embryo sac, placenta
(b) Thalamus, pistil, style, ovule
(c) Ovule, ovary, embryo sac, tapetum
(d) Ovule, stamen, ovary, embryo sac
Answer:
(a) Stigma, ovule, embryo sac, placenta

Question 21.
Science of cultivation, breeding, marketing and arrangement of flowers is called
(a) arboriculture
(b) floriculture
(c) horticulture
(d) anthology
Answer:
(b) floriculture

Question 22.
Nonessential floral organs in a flower are
(a) sepals and petals
(b) anther and ovary
(c) stigma and filament
(d) petals only.
Answer:
(a) sepals and petals

Question 23.
The stamens represent
(a) microsporangia
(b) male gametophyte
(c) male gametes
(d) microsporophylls.
Answer:
(d) microsporophylls

Question 24.
Anther is generally
(a) monosporangiate
(b) bisporangiate
(c) letrasporangiate
(d) trisporangiate.
Answer:
(c) letrasporangiate

Question 25.
The anther wall consists of four wall layers where
(a) tapetum lies just inner to endothecium
(b) middle layers lie between endothecium and tapetum
(c) endothecium lies inner to middle layers
(d) tapetum lies next to epidermis.
Answer:
(b) middle layers lie between endothecium and tapetum

Question 26.
The innermost layer of anther is tapetum whose function is
(a) dehiscence
(b) mechanical
(c) nutrition
(d) protection.
Answer:
(c) nutrition

Question 27.
Callase enzyme which dissolves callose of pollen tetrads to separate four pollens is provided by
(a) pollens
(b) tapetum
(c) middle layers
(d) endothecium.
Answer:
(b) tapetum

Question 28.
In angiosperms various stages of reductional division can best be studied in
(a) young anthers
(b) mature anthers
(c) young ovules
(d) endosperm cells.
Answer:
(a) young anthers

Question 29.
Study of pollen grains is called
(a) micrology
(b) anthology
(c) palynology
(d) pomology
Answer:
(c) palynology

Question 30.
Several pollen grains form a unit designated as pollinium in Family
(a) Asteraceae
(c) Asclepiadaceae Pollen
(b) Cucurbitaceae
(d) Brassicaceae
Answer:
(c) Asclepiadaceae Pollen

Question 31.
Triple fusion in Capsella bursa pastoris is fusion of male gamete with
(a) egg
(b) synergid
(c) secondary nucleus
(d) antipodal.
Answer:
(c) secondary nucleus

Question 32.
Double fertilisation was first discovered in 1898 by _______ in Fritillaria and Lilium.
(a) Nawaschin
(b) Strasburger
(c) Amici
(d) Focke
Answer:
(a) Nawaschin

Question 33.
If an endosperm cell of an angiosperm contains 24 chromosomes, the number of chromosomes in each cell of the root will be
(a) 8
(b) 4
(c) 16
(d) 24
Answer:
(c) 16

Question 34.
The cells of endosperm have 24 chromosomes. What will be the number of chromosomes in the gametes ?
(a) 8
(b) 16
(c) 23
(d) 32
Answer:
(a) 8

Question 35.
The true embryo develops as a result to fusion of
(a) two polar nuclei of embryo sac
(b) egg cell and male gamete
(c) synergid and male gamete
(d) male gamete and antipodals.
Answer:
(b) egg cell and male gamete

Question 36.
Father of Indian embryology is
(a) P. Maheshwari
(b) Swaminathan
(c) R. Misra
(d) Butler
Answer:
(a) P. Maheshwari

Question 37.
The portion of embryonal axis between plumule (future shoot) and cotyledons is called
(a) hypocotyl
(b) epicotyl
(c) coleorhiza
(d) coleoptile.
Answer:
(b) epicotyl

Question 38.
Coleoptile and coleorhiza are the protective sheaths _______ covering _______ and _______ respectively.
(a) plumule, epicotyl
(b) radicle, plumule
(c) plumule, radicle
(d) radicle, hypocotyl
Answer:
(c) plumule, radicle

Question 39.
_______ is not an endospermic seed.
(a) Pea
(b) Castor
(c) Maize
(d) Wheat
Answer:
(a) Pea

Question 40.
Endosperm is completely consumed by the developing embryo in
(a) pea and groundnut
(b) maize and castor
(c) castor and groundnut
(d) maize and pea.
Answer:
(a) pea and groundnut

Question 41.
Pollen grain is a
(a) megaspore
(b) microspore
(b) microspore
(d) microsporangium.
Answer:
(b) microspore

Question 42.
How many pollen mother cells should undergo meiotic division to produce 64 pollen grains ?
(a) 64
(b) 32
(c) 16
(d) 8
Answer:
(c) 16

Question 43.
How many meiotic divisions are required for the formation of 100 pollen grains ?
(a) 100
(b) 50
(c) 25
(d) 26
Answer:
(c) 25

Question 44.
One of the most resistant biological material present in the exine of pollen grain is
(a) pectocellulose
(b) sporopollenin
(c) suberin
(d) cellulose.
Answer:
(b) sporopollenin

Question 45.
What is the function of germ pore ?
(a) Emergence of radicle
(b) Absorption of water for seed germination
(c) Initiation of pollen tube
(d) All of these .
Answer:
(c) Initiation of pollen tube

Question 46.
_______of the pollen grain divides to form two male gametes.
(a) Vegetative cell
(b) Generative cell
(c) Microspore mother cell
(d) None of these
Answer:
(b) Generative cell

Question 47.
The three cells found in a pollen grain when it is shed at 3-celled stage are
(a) 1 vegetative cell, 1 generative cell, 1 male gamete
(b) 1 vegetative cell, 2 male gametes
(c) 1 generative cell, 2 male gametes
(d) either (a) or (b).
Answer:
(b) 1 vegetative cell, 2 male gametes

Question 48.
Megasporangium along with its protective integuments is called
(a) ovary
(b) ovule
(c) funicle
(d) chalaza
Answer:
(b) ovule

Question 49.
Mature ovules are classified on the basis of funiculus. If micropyle comes to lie close to the funiculus the ovule is termed as
(a) orthotropous
(b) anatropous
(c) hemitropous
(d) campylotropous
Answer:
(b) anatropous

Question 50.
When micropyle, chalaza and hilum lie in a straight line, the ovule is said to be
(a) anatropous
(b) orthotropous
(c) amphitropous
(d) campylotropous.
Answer:
(b) orthotropous

Question 51.
Fragrant flowers with well developed nectaries are an adaptation for
(a) hydrophily
(b) anemophily
(c) entomophily
(d) none of these
Answer:
(c) entomophily

Question 52.
Pollen kitt is generally found in
(a) anemophilous flowers
(b) entomophilous flowers
(c) ornithophilous flowers
(d) malacophilous flowers
Answer:
(b) entomophilous flowers

Question 53.
Which of these is a condition that makes flowers invariably autogamous ?
(a) Dioecy
(b) Self incompatibility
(c) Cleistogamy
(d) Xenogamy
Answer:
(c) Cleistogamy

Question 54.
Heterostyly as a contrivance for cross-pollination is found in
(a) Pennisetum
(b) Impatiens
(c) Primula vulgaris
(d) Oenothera
Answer:
(c) Primula vulgaris

Question 55.
The part of gynoecium that determines the compatible nature of pollen is
(a) stigma
(b) style
(c) ovary
(d) synergids
Answer:
(a) stigma

Question 56.
Part of the gynoecium which receives the pollen is called
(a) style
(b) stigma
(c) ovule
(d) ovary
Answer:
(b) stigma

Question 57.
Growth of pollen tube towards embryo sac is
(a) chemotropic
(b) thigmotaxis
(c) geotropic
(d) none of these
Answer:
(a) chemotropic

Question 58.
During the process of fertilisation the pollen tube of the pollen grain usually enters the embryo sac through
(a) integument
(b) nucellus
(c) chalaza
(d) micropyle
Answer:
(d) micropyle

Question 59.
Fusion of one of the male gametes with egg nucleus is referred to as
(a) generative fertilisation
(b) syngamy
(c) vegetative fertilisation
(d) both (a) and (b)
Answer:
(d) both (a) and (b)

Question 60.
The total number of nuclei involved in double fertilisation in angiospersm are
(a) two
(b) three
(c) four
(d) five
Answer:
(d) five

We hope the given Biology MCQs for Class 12 with Answers Chapter 2 Sexual Reproduction in Flowering Plants will help you. If you have any query regarding CBSE Class 12 Biology Sexual Reproduction in Flowering Plants MCQs Pdf, drop a comment below and we will get back to you at the earliest.


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Background

The ability to tailor growth and development to prevailing environmental conditions is a key feature of plant biology and has been instrumental in the successful colonization of all terrestrial biospheres by plants. Plant growth is coordinated in space and time through the production and systemic transport of plant hormones external modulation of these signals allows coupling of environment and development. Strigolactones (SLs) are a class of carotenoid-derived signalling molecules which function endogenously as hormones, while also acting in an exogenous manner as signals in the rhizosphere (reviewed in [1]). SLs play a key role in multiple developmental pathways, including the regulation of shoot branching, lateral root formation and leaf growth. Additionally, the exudation of SLs from the roots into the soil has been shown to be a key factor for the recruitment of arbuscular mycorrhizal (AM) fungi [2]. SLs are particularly associated with soil phosphate levels, SL synthesis is upregulated in low phosphate conditions [3] and the subsequent recruitment of AM fungi provides the plant with phosphate in exchange for reduced carbon. A proportion of the SLs synthesized within the root are transported into the shoot system, where an inhibitory effect on shoot branching allows the plant to modify shoot system size in direct relation to the availability of soil-borne resources [4].

In flowering plants (angiosperms), the synthesis of SLs is carried out by a core pathway of four enzymes, which have been characterized in multiple species (reviewed in [1]). The initial substrate all-trans-β-carotene is processed by the carotene isomerase DWARF27 (D27) to 9-cis-β-carotene [5], which is subsequently cleaved and modified by two carotenoid cleavage dioxygenases (CCD7 and CCD8) in turn [5]. The resulting product, carlactone (CL), is the common precursor for all known SLs, but must be modified by cytochrome P450 enzymes of the MAX1 family to form carlactonoic acid (CLA) or other active derivatives [6, 7]. These intermediates are thought to be further processed by an array of enzymes that result in a diverse set of active SL structures (e.g. [8]). In Arabidopsis, LATERAL BRANCHING OXIDOREDUCTASE (LBO) has been identified as late-acting enzyme that converts CLA to methyl-CLA (MeCLA), but it assumed further enzymes must also exist, as MeCLA is not an abundant naturally occurring SL in Arabidopsis [8]. SL signalling is mediated by the DWARF14 (D14) α/β hydrolase receptor, which can both bind and hydrolyse SLs the relative importance of hydrolysis in signalling is still an open question [9,10,11,12]. SL binding triggers a conformational change in D14 that mediates its interaction with MAX2, an F-box protein that forms part of an SCF ubiquitin ligase complex, which targets proteins for proteolytic degradation [9,10,11]. The target proteins of D14 are members of the HSP101-like SMAX1-LIKE family, specifically the SMAX1-LIKE7/DWARF53 (SMXL7/D53) sub-family. Recruitment of SMXL7 proteins to the signalling complex by active D14 results in the ubiquitination and subsequent degradation of both the D14 and SMXL proteins [13,14,15,16]. Turnover of SMXL7 proteins allows downstream SL responses to occur, which seem to include both removal of the PIN1 auxin efflux carrier from the plasma membrane of cells in the stem [15, 17, 18] and increased transcription of BRANCHED1-type transcription factors [15, 16, 19, 20]. SMXL proteins are not DNA-binding transcription factors, but have a well-conserved ERF-associated repressive (EAR) motif, and have thus been proposed to act as intermediates in the assembly of repressive transcriptional complexes, via recruitment of TOPLESS family chromatin remodelling complexes [21]. There is some evidence for this, particularly in rice [22], but generally transcriptional responses to SL are limited [23], and the EAR motif is not absolutely required for SMXL7 function [17]. The function of SMXL proteins thus remains rather enigmatic, and it is possible that they have multiple cellular functions, both transcriptional and non-transcriptional.

The evolution of SL synthesis and signalling has generated equal amounts of interest and confusion. It is clear that this evolution history is not simple, with different components appearing at different points in the evolutionary record [1]. For instance, with regard to SL synthesis, it has been proposed that D27 arose in the algal ancestors of land plants, CCD7 at the base of the land plant group, CCD8 after the divergence of liverworts and other land plants, MAX1 within the vascular plant group and LBO specifically within seed plants [1, 8, 24, 25]. Outside flowering plants, SL synthesis has been characterized in the moss Physcomitrella patens, where CCD7 and CCD8 act consecutively in CL synthesis as in angiosperms [26, 27]. There is some uncertainty about which strigolactones are ultimately synthesized by P. patens, with recent analysis suggesting only CL is produced, consistent with the lack of MAX1 orthologue in this species [27, 28]. In general, conclusions regarding SL synthesis outside the angiosperms are based on very limited sampling of sequences. Conversely, a more exhaustive approach to sampling has recently demonstrated that SL signalling via canonical D14-type SL receptors appears to be a relatively recent innovation within the seed plants [29]. Understanding the evolution of SL signalling is complicated by the apparent origin of the signalling pathway through duplication of an existing pathway. D14 proteins are closely related to the KARRIKIN-INSENSITIVE2 (KAI2) sub-family of α/β hydrolases and appear to have arisen by duplication of KAI2 near the base of land plants followed by gradual neo-functionalization [29]. KAI2-like proteins are found in charophyte algae, indicating a very ancient origin for KAI2 itself [29]. In angiosperms, KAI2 acts in the perception of smoke-derived karrikin molecules in the environment, but it is also assumed to act as a receptor for an as-yet-unidentified endogenous compound (KAI2-Ligand, KL) (reviewed in [1]). Both D14 and KAI2 signalling act through SCF MAX2 [30] MAX2 itself has an ancient origin in the algal ancestors of land plants [29]. SMXL7 proteins are also closely related to the presumptive targets of KAI2 signalling, members of the SUPPRESSOR OF MAX2 1 (SMAX1) sub-family of the SMXL family [31, 32], and it has recently been suggested that the SMXL7 sub-family may also be a relatively recent innovation in plants [33].

The evolution of SLs thus represents something of enigma, but the evidence is currently highly fragmentary, and based on limited sampling from non-representative genomes. In order to try and unravel this mystery, we have exploited recently generated genomic and transcriptomic sequences from across the land plant clade, to reassess the distribution and evolutionary history of synthesis and signalling components in land plants.


Methods

Study Site and Dataset.

This study was conducted at the Rocky Mountain Biological Laboratory (RMBL) in the Colorado Rocky Mountains, USA (38°57.5′N, 106°59.3′W, 2,900 m above sea level). For each of the 121 flowering plant species that occur in our thirty 2 × 2 m plots, either the number of flowers per stalk or the number of flowering inflorescences (for species with many small flowers) were counted every other day throughout the growing season from 1974–2012. Copies of the flowering phenology dataset and metadata are archived at www.rmbl.org and in the Digital Repository at the University of Maryland (http://drum.lib.umd.edu/). We limited the analysis to species that were present in at least half of the years of the dataset (19 y), leaving a total of 60 species that represent the meadow plant communities in and around the RMBL (see ref. 10 for more information about plant species). There was no census in 1978 and 1990. Thus, there was a maximum of n = 37 y for each species, and a minimum of n = 19 y because not all species flower in every year. Five of the 30 plots were added in later years: two in 1985 and three in 1998. The addition of five plots should not alter estimates of phenological change, because the magnitude of phenological change generally is not affected by changes in peak floral abundance (Table S2). Furthermore, we find no relationship between changes in peak floral abundance and shifts in the timing of peak flowering for the 60 species studied here (r = 0.038, n = 60 species). These five plots were excluded from analyses that used floral abundance: species-level change in peak floral abundance, coflowering patterns, and aggregate community-level responses. Records for the annual timing of snowmelt come from a permanent 5 × 5 m snow plot at the RMBL in which the first day of bare ground is recorded as the date of snowmelt. Mean temperatures used in analyses are the average of the daily minimum and maximum temperatures at the Crested Butte National Oceanic and Atmosphere Administration weather station (ca. 9 km south of the RMBL).

Species-Level Analyses.

For each species, the number of flowers was summed across all 30 plots on each census day to create one annual flowering distribution per species. First flowering was the first day on which a flower for that species was observed, and last flowering was the last day on which a flower was observed, taken from the across-plot sum. Peak flowering for individual species was the day on which 50% of the flowers were counted (following refs. 9 and 10). Peak floral abundance was the maximum number of flowers counted annually in one census. Years in which the census started late (1976, 1982, 1985, 1992, and 1994) were excluded from analysis when the response variable of interest was affected (first flowering and occasionally peak flowering for the earliest-flowering species). Linear regression was used to analyze change through time, with phenology or peak floral abundance as a response and year as a continuous predictor. We tested for temporal autocorrelation in the time series of species showing significant phenological change through time, using the Ljung–Box test with a lag time of 1 y. We found evidence of significant temporal autocorrelation in only three cases (Table S5). We reanalyzed these three cases with an autoregressive linear model, which allows the error structure to be correlated. The rates of change in these models were very similar to the rates of change in our simple linear regression analysis, and change through time was still significant in all three cases (Table S6). We therefore conclude that temporal autocorrelation in this dataset does not bias our results.

To determine whether phenological shifts could have been an artifact of changes in peak floral abundance (14), we ran correlation analyses for species showing significant shifts in both phenology and peak floral abundance (defined as the maximum number of flowers counted annually in a census for individual species). We looked for increasing peak floral abundance in correlation with earlier first flowering and later last flowering we also looked for decreasing peak floral abundance in correlation with later first flowering and earlier last flowering. These relationships indicate the possibility of detecting what appears to be a phenological shift that actually is caused by a change in flower abundance (14). We assume that changes in peak floral abundance are indicative of changes in floral abundance because we do not track individual flowers through time. There is no mathematical reason to expect a change in peak abundance to alter the probability of detecting for shifts in the timing of peak flowering.

A thorough analysis of associations of temperature and snowmelt with first, peak, and last flowering has been presented elsewhere interannual variation in temperature and the timing of snowmelt independently account for a significant amount of variation in first, peak, and last flowering in 93–98% of the species in this study, depending on the flowering response (10). To ensure that our conclusions about phenological predictions based on change through time are not affected by using sensitivities to climate variables in place of year, we used linear regression to assess how well sensitivity of first flowering to climate predicts sensitivity of peak and last flowering to climate (Table S3).

Interaction Potential.

For each year, coflowering was calculated as the number of flowers of every pair of species that overlap in time, weighted by the total number of flowers of the focal species. For each pair of species, the minimum number of open flowers of the two species was summed on each census day, representing the total number of flowers for the two species that were open at the same time. We then weighted this minimum value by the total number of flowers for each species in each year, so that coflowering values represent overlap relative to each species’ annual floral abundance. For example, the total number of Claytonia lanceolata and Mertensia fusiformis flowers that overlapped through time in 2012 was 633. A total of 3,909 C. lanceolata flowers were counted across all plots in this season, compared with 1,287 flowers of M. fusiformis. C. lanceolata’s flowering overlap score with M. fusiformis was 633/3,909 (0.162), and M. fusiformis’ overlap with C. lanceolata was 633/1,287 (0.492). These calculations resulted in 3,540 potential overlap scores for each year (a matrix of 60 species by 60 species, minus the diagonal of same-species interactions). Linear regression was run for each pair of species to examine the amount of change in coflowering overlap through time. We conducted a permutation test of 5,000 runs to obtain P values for each regression. Because we already have shown that species-specific phenological shifts are strongly associated with climate (10), we did not analyze the response of coflowering to climate.

Aggregate Community-Level Phenology.

Floral abundance was summed across all species and plots on each census day for each year to create an annual community-level phenology curve. Linear regression was used to assess changes in community phenology (first day of flowering, day of spring peak flowering, day of summer peak flowering, last day of flowering, and flowering duration) and community-level floral abundance (spring and summer maximum number of flowers, total number of flowers counted, and average number of flowers counted per census) through time. The onset of the flowering period was missed in 12 y because the census started after flowering had already begun in some of the earliest-flowering plots. In five of these years (1974, 1976–77, 1992, and 1994), peak abundance of the first species to flower and an important component of spring peak flowering, C. lanceolata was missed also. These 5 y were excluded from analysis of flowering season length, timing and abundance of spring peak, and start of the flowering season (similar to species-level analyses). For the remaining 7 y (1979, 1982–1983, 1985–1986, 1991, and 1993), we estimated the start of the flowering season based on the slope of a line of flower accumulation from years with known start dates and similar floral abundance. We applied the same procedure to estimate the end of the flowering season for 5 y in which the end of the flowering season was missed (1976–1977, 1984, and 1992–1993). We used ANCOVAs to verify that these estimations did not bias our results by comparing the slopes of regressions using estimated vs. missing values (Table S7).

Two community-level peaks in floral abundance were clearly evident in almost every year, with the exception of 4 y that were excluded from analysis (1985, 1987, 1994, and 2012) (Fig. 4A) (7). Additionally, in 5 y (1989, 1991–92, 2002, and 2007) there was some evidence of a third peak in floral abundance between the spring and summer peaks. We determined the summer peak in these years based on the species that typically compose the summer peak of floral abundance. There was virtually no turnover in species present in the first and last 10 y of the dataset (Fig. 4A), although Pedicularis bracteosa was absent in the last 10 y of the dataset. Because this species is relatively rare in this community, we do not expect its absence to affect the community-level patterns shown in Fig. 4A.


Watch the video: MORPHOLOGY IN FLOWERING PLANTS lecture #1 (August 2022).