How do lilies sense day and night and open and close their flowers?

How do lilies sense day and night and open and close their flowers?

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We have lots of lily flowers inside our garden. Their flowers are open in day and closed in night. How do lilies sense day and night and open and close their flowers?

The three main cues for flower opening/closing used by plants are temperature, light and humidity (van Doorn & van Meteren 2003, freely available pdf), with the first two being most common. Plants with daily opening and closing of flowers can be divided into nocturnal (open at night) and diurnal (open at day). There exists several different mechanisms for how flowers open and close, and these include e.g. reversible expansion and contraction of cells by changes in water balance and differential growth of cells due to temperature (in either the petals themselves or cells at the base of flowers). See the previously referred paper for examples.

The evolutionary advantages and molecular mechanisms (along with the circadian clock of plants) behind opening and closing of flowers are open research fields. Several evolutionary hypothesis exists for explaining different flowering strategies, and these often deal with efficient pollination (close when good pollinators are absent), protection against frost, conservation of resources (e.g. water) or predator/pathogen defence.

I do not know what the specific mechanism in lilies is, and it can possibly/probably differ between different species.

Us vs. them

Seven areas of greatest friction you and your GM will wrestle with, and how to fix them now before you’re down for the count.

The relationship between a golf course superintendent and the general manager can be likened to a marriage of sorts. Two people coming together and working as a team. Inevitably there will be a honeymoon period that is pure bliss, but there will also be times that are challenging over the years together. Marriages remain strong because people work at it. Each individual knows their role and also knows what makes the other person happy. Such it is in so many ways with the golf course superintendent and general manager relationship.

There was a time in which many clubs operated with independent department heads, but that has long been trending toward the general manager/COO concept and many superintendents find themselves reporting to a general manager rather than a green chairman or directly to a club’s board of directors. The general manager needs the superintendent to perform their magic and the superintendent needs the GM to help get things approved and be supportive of the initiatives of the department. Similar to a marriage, it is a give-and-take proposition. When a relationship works there is nothing better, but when it sours it becomes difficult for people to work with each other. If a superintendent does not have the respect and support of his general manager, then it is likely that a job change is on the horizon.

Advancing your career

Some superintendents desire a long career at the facility where they work and stay there for decades. Others choose to move up the career ladder and move on to greater responsibilities and much higher compensation levels. I have found that the general manager can be so important in helping the superintendent in his career advancement.

I consider all of the managers who I have worked with and the general managers that I have worked for as key people in mentoring me over the years. Watching, listening, learning from how they manage people and handle leadership responsibilities has been important. Those GMs that take the time and have an active interest in helping your grow are the best kind of people to work for.

What are your existing skills and what skills might you need to move on in your career? The gap that might exist can be learned when given opportunities to take on more responsibility or learn new skills through external education and support of networking opportunities and service through industry associations.

Some of my peers have attained certifications, received graduate degrees, learned a new language and managed other departments and projects beyond the normal scope that they were hired for. All of that bodes well to advance within the organization you work for or if you will need those skills on your next job.

To understand what makes for a great relationship it is important to know the areas of greatest friction between these two key management positions at a golf course.

1. Communication

More superintendents lose their jobs over an inability to communicate than over an inability to grow grass.

It is extremely important to meet with the general manager as often as possible in a formal setting to discuss what has been accomplished and also what is planned for the days, weeks and months ahead. Knowing what the membership/players want is often expressed through membership comments to the board of directors or general manager directly. Like it or not it is imperative that they be shared. Through proper communication the general manager can become an advocate of the department and the work that is being done to meet or exceed expectations.

2. Understanding club goals
Golf course superintendents are trained to provide exceptional golf course conditions. Anything that stands in the way of that is counter-culture to most superintendents’ way of thinking. However, the goals of the club are more important than the goals of any one department head. Superintendents should never put the goals of the department ahead of the goals of the business. While tee times with 7-minute intervals or hosting Monday outings may not be met with open arms by superintendents, if they provide the finances that support an operating budget and buy adequate equipment then it all contributes to the success of the facility.

3. Interdepartamental collaboration

A general manager who I worked for told me how important it was for his department heads and departments to get along. One of the roles of the general manager is to keep as many people happy in the organization as possible. With any type of disharmony this can create major problems for the GM. The golf professional, superintendent, chef, HR department head, controller and all must work cohesively. Superintendents should go out of their way to make this happen.

4. Team concept
There is an old adage of “together we win and divided we fall.” Every department is a part of the success of the operation of a club. From the receptionist at the front desk to the locker room attendant each and every person and department adds to the experience of a member. Thoughts of giving blame to others and compartmentalizing things with the thought of “that’s not my job” will encumber operations and develop ill will in the organization.

5. Budget Adherence

It should always be important for any department head to meet their budget expectations. Clubs are a business. General managers run the business and are often judged partially on adherence to the overall club budget. Golf course maintenance is a big figure in that overall club budget. Many managers are given a bonus that has a component they are graded on for meeting their forecasted budget. When the golf course superintendent’s portion of the overall budget is greater than forecast then it could cost the manager some money.

6. Loyalty
In a beautiful relationship there is a huge amount of trust between the superintendent and GM. There are often private discussions of a sensitive nature and those comments need to be considered privileged information. There will be times to disagree behind closed doors but it is very important that the two individuals be supportive of each other and work with a united front when dealing with the board and committees.

7. Professional animosity

Nobody likes to talk about it but egos can get in the way of superintendents and GMs. There is no room for this and ultimately it is seldom that a superintendent will win the battle of egos. Set the egos aside. If the facility succeeds there is plenty of room for accolades for all and that often ends in above-average compensation or bonuses.

Making the magic. If we know what the major potential issues are in a relationship then what can be done to be sure the honeymoon lasts forever? Several ideas that will work should be put on a checklist to evaluate each and every year.

For more
Check out this issue’s app version, as well as the Superintendent Radio Network, for an exclusive podcast between SRN Host Kyle Brown and Bruce Williams that continues the discussion about how to improve your relationship with not only your general manager, but with other department heads at your facility.

As a superintendent use effective communication with weekly meetings with the GM. It is best to also play the golf course or at least tour it so there are no surprises. I have never met a general manager that likes surprises. Hearing about a mainline break in the irrigation system should not come from golfers but be reported immediately to the front office. With today’s technology we can be in touch almost instantaneously with our supervisors.

Early on in my career I was told of a general manager that had a plaque on her wall, behind her desk, that said “Bring Me Solutions, Don’t Bring Me Problems.” Any superintendent that follows that premise will surely have a great relationship with their GM.

Be sure to understand the mission, vision and goals of the facility. This should be shared with your staff and explained thoroughly to all new hires. If those items don’t exist then departments may be headed in different directions and the left hand won’t know what the right hand is doing.

Check your ego at the door. I worked for a wonderful GM in Jim Brewer who was at LACC for 37 years. Not a day went by in which I would tell myself that I was entering Mr. Brewer’s kingdom and he was King! He was the boss and I had the utmost respect for him. The buck stopped with him and while we both were well respected in our industries there was no room for any level of discord. Department heads worked in unison and that was all a part of what made The Los Angeles Country Club the great club that it was.

The benefits

Some of the benefits of a strong relationship have been discussed. But none is more important than having the general manager serve as an advocate for the golf course superintendent.

Each club has a different governance structure but most utilize the general manager as the conduit for information from department heads to the board of directors, finance committee, etc. Therefore the GM should be serving as an advocate and spokesperson to advance the needs of the greens department.

If the superintendent communicates effectively, is a team player, is loyal and runs his department with fiscal prudence then it is likely that the GM will carry the proper message to the leadership of the club to get the resources required to meet the goals and expectations of the club.

Budgets are guidelines that a superintendent tries to adhere to. Through the use of proper purchasing, labor management and resource management most years’ budgets should be met. In the years disasters take place, or unexpected circumstances, then it is important the GM be informed monthly of any variances and also if the board needs to make overall adjustments due to down revenues.

Loyalty is not something that you can turn on or off. You are either loyal or you are not. Be honest and be supportive. It is very important to be there working alongside the GM not only when times are good but when they are bad as well. Be the go to guy that gets it done. When the superintendent is the guy you can count on and also the guy that has your backside covered it is the glue that holds the relationship together.

Ties that bind. The happiest of superintendents are those people who love going to work each and every day. A major part of that is liking the people you work with and who you work for.

We don’t always get to choose who we work for but we all get to choose whether or not we want to make that relationship work. There are so many upsides for you, your career and the success of the facility to not want to work hard to make the superintendent and general manager relationship work. Make it a priority each and every day and you won’t be disappointed.

Bruce Williams, CGCS, is principal for both Bruce Williams Golf Consulting and Executive Golf Search. He’s GCI’s senior contributing editor.

Biology Study Guide Chapter 17 + 31 + 33

A student taking a plant physiology class is interested in investigating what will happen if the apical bud is removed from a growing plant and supplementary hormones are introduced.

He set up his experiment with two groups of plants of the same species. In groups A and B, the apical buds were removed and the cut apical ends were wrapped with hormone-impregnated cotton. The plants were observed over a five-week period for growth and development. In group A, many axillary buds and leaves appeared along the sides of the stem, but the plants had minimal root growth. In group B, minimal growth occurred in the shoot and roots, and no axillary buds formed.

2. root tissues are more sensitive than stem tissues

1.Shoots showed negative gravitropism.

2.Roots showed positive gravitropism.

3.Root cap was responsible for sensing.

Later it was shown that . . .
Auxin was the main hormone involved.
Amyloplasts acted as statoliths.


With the success of the triose phosphate/phosphate antiporter (TPT) in explaining carbon export from chloroplasts during the day, it was natural to assume that carbon export at night was similar. Maltose as a degradative product of starch was first reported by Levi & Gibbs (1976 ). Later, it was reported that the principal products of starch breakdown in the presence of phosphate were triose phosphate and 3-phosphoglycerate, and that starch was also converted to maltose and glucose in a phosphate-independent reaction ( Heldt et al. 1977 Peavey, Steup & Gibbs 1977 Stitt & ap Rees 1980 Stitt & Heldt 1981b ). However, Kruger & ap Rees (1983 ) reported that the absence of exogenous phosphate substantially reduced starch breakdown and maltose accumulation by isolated pea (Pisum sativum) chloroplasts. Nevertheless, it was concluded that the products of starch breakdown in spinach chloroplasts included triose phosphate, 3-phosphoglycerate, CO2, glucose and maltose ( Stitt & Heldt 1981a ). Phosphorolytic breakdown of starch was favoured ( Stitt et al. 1978 Stitt & ap Rees 1980 Stitt & Heldt 1981a ), although it was suggested that some carbon from starch degradation was exported as hexose or maltose ( Stitt et al. 1985 ).

Interest from this lab in starch degradation started with the discovery of a mutant of Flaveria linearis lacking cytosolic fructose bisphosphatase (FBPase). Compared to wild-type plants, these plants partitioned more of their photosynthate into starch and less into sucrose during the day these plants also did not export carbon from their leaves during the day ( Sharkey et al. 1992 ). However, during the night the rate of starch mobilization in the leaves of the mutant plants was twice the rate in wild-type plants ( Sharkey et al. 1992 ). This indicated that there was a different pathway for exporting carbon from chloroplasts that did not rely on cytosolic FBPase but only operated at night. The presence of a distinct night-time carbon export pathway was confirmed using plants in which cytosolic FBPase activity was reduced by antisense technology ( Zrenner et al. 1996 ). When the TPT was reduced by antisense, the same reduction in daytime carbon export and an increase in night-time export was observed ( Heineke et al. 1994 ). These works all led to the conclusion that there was a pathway for starch conversion to sucrose that did not involve the TPT or cytosolic FBPase and that could operate at night but not during the day.

The question arose ‘is the alternate night-time pathway induced only when the TPT export pathway is blocked or is it the normal night-time pathway?’ By feeding deuterium-enriched water to leaves at night, Schleucher, Vanderveer & Sharkey (1998 ) were able to show that plants which had no genetic modifications also used the alternative pathway for carbon export at night. Deuterium was incorporated at C2, as expected because of interconversion of fructose 6-phosphate (F6P) and glucose 6-phosphate (G6P), but was not incorporated into locations indicative of triose phosphate metabolism. The conclusion of these studies was that there were two independent pathways for carbon export from chloroplasts, one involving triose phosphates that operated during the day and one involving hexoses (or higher order polymers) that normally operated at night. Surprisingly, plants can grow well relying exclusively on either pathway, although optimum growth requires both. If both pathways were blocked, plant growth was severely reduced ( Hattenbach et al. 1997 ).

This conclusion fits with data on cytosolic FBPase. At night, cytosolic FBPase activity is severely reduced by the presence of fructose 2,6-bisphosphate ( Herzog, Stitt & Heldt et al. 1984 ). These authors concluded that ‘if the cytosolic FBPase is inactive in the dark, it is unclear how starch can be converted to sucrose by a route involving starch phosphorolysis followed by release of PGA or triose phosphate from the chloroplast, which are then converted to sucrose in the cytosol by a path analogous to that in the light’. Nevertheless, it would be another 20 years before the answer to that conundrum, an alternative pathway of carbon export at night, was widely accepted.

Sucrose-phosphate synthase can be in a less active form at night ( Sicher & Kremer 1984 Huber & Huber 1996 ) but its activity is not zero ( Hendrix & Huber 1986 ), while cytosolic FBPase activity does go to zero. Therefore, a pathway of carbon export that bypassed triose phosphate and cytosolic FBPase could deliver carbon that could be converted to sucrose so that carbon could be exported from leaves at night.

The nuclear magnetic resonance (NMR) data proved that the carbon exported at night was never broken down to triose phosphates ( Schleucher et al. 1998 Niewiadomski et al. 2005 ). But what was the primary export compound(s)? Plastids have a hexose phosphate transporter, but this is normally expressed only in heterotrophic tissues ( Kammerer et al. 1998 ) and perhaps in crassulacean acid metasolism (CAM) tissues ( Neuhaus & Schulte 1996 ). In addition to glucose, higher maltodextrins such as maltose or malotriose might also be exported and provide an energetic advantage over export of glucose ( Weise & Sharkey 2004 ). It was known that the chloroplast is permeable to maltose (but not higher maltodextrins) ( Schäfer, Heber & Heldt 1977 Rost, Frank & Beck 1996 ).

Silicon oil centrifugation techniques were used to separate chloroplasts from the incubation medium following starch degradation in the dark. By removing the chloroplasts from the incubation buffer, it was possible to measure what was exported, but not all of the products of starch breakdown. These experiments are difficult because of the need to isolate intact, starch-laden chloroplasts. Nevertheless, these experiments did provide the correct answer, as subsequently confirmed by genetic analysis (below). It was reported by different groups that maltose and glucose are the two major forms of carbon exported from chloroplasts during starch degradation ( Servaites & Geiger 2002 Ritte & Raschke 2003 Weise, Weber & Sharkey 2004 ). Servaites & Geiger (2002 ), using a maltase assay, concluded that one-third of the carbon could be isomaltose (α 1,6 linked glucose). Weise et al. (2004 ) used high-performance liquid chromatography (HPLC) plus a more specific maltose phosphorylase assay and concluded that no isomaltose nor maltotriose or higher maltodextrin was exported. Between two-thirds and four-fifths of the carbon exported at night was exported as maltose most of the rest exported as glucose. Maltose was confirmed to be a major product of catabolism of starch in guard cells as well ( Ritte & Raschke 2003 ).

The essential role of maltose was confirmed by finding the maltose transporter in the chloroplast membrane ( Niittyläet al. 2004 ) and the first enzyme that metabolizes maltose in the cytosol, disproportionating enzyme (D-enzyme) 2, DPE2 ( Chia et al. 2004 Lu & Sharkey 2004 ). Plants that lack either of these proteins accumulate as much as 100 times the normal level of maltose.


This work was supported by the College of Agricultural and Life Sciences of the University of Wisconsin and by a grant to R.A. from the National Science Foundation. M.R.D. was supported by a Molecular Biosciences Training Grant (NIH) R.M.B. was supported by a Gatsby graduate studentship S.J.D. is a Department of Energy Bioscience fellow of the Life Sciences Research Foundation. Work in Warwick was supported by grants from the Biotechnology and Biological Sciences Research Council and the Human Frontier Science Program (HFSP) to A.J.M. The work in Hungary was supported by the Howard Hughes Medical Institute.


We had previously uncovered a role for CRY in fly visual biology, by the interaction with the phototransduction cascade (Mazzotta et al., 2013). Here, we show that through this interaction it also slightly increases light-sensitivity of the eyes, and WT flies may sense day-light, nocturnal light and red light as being brighter than cry 01 mutants do. This role of CRY in the fly retina is rather independent of its function as photopigment, as CRY seems to act as a stabilizing protein keeping the INAD signalplex linked to the F-actin and therefore to the rhabdomere internal membrane.

This non-photoreceptive role of CRY in the retina could be a feature shared with mammals. In fact, mammalian CRYs are expressed in the retina, especially in the ganglion cells responsible for circadian entrainment and pupillary responses (Thresher et al., 1998 Thompson et al., 2003). Nowadays, it is clear that melanopsin—not CRYs—in the retinal ganglion cells is the major mammalian circadian photopigment (Hattar et al., 2002 Panda et al., 2002 Ruby et al., 2002 Lucas et al., 2003 Peirson and Foster, 2006). Nevertheless, several reports suggest that CRYs affect circadian photoreception and pupillary responses (Miyamoto and Sancar, 1998 Selby et al., 2000 Van Gelder et al., 2003). Also, mammalian CRYs could stabilize the phototransduction complex at the membrane of retinal cells. This is conceivable because melanopsin ganglion cells have an insect-like (rhabdomeric) phototransduction cascade employing Gq/11-class G proteins and Phospholipase C (PLC Graham et al., 2008). This tempting hypothesis is reinforced by our finding that human CRY2 is able to interact with human Actin-Beta in a light-independent manner.

The role for CRY we propose here is new and clearly different from the recently shown CRY action at the membrane of the large lateral ventral neurons, where light-activated CRY evokes rapid membrane depolarization through the redox sensor of the voltage-gated ß-subunit potassium channel hyperkinetic (Fogle et al., 2015). Though, we cannot completely exclude such a role for CRY in the photoreceptor cells, our results rather speak for a role of CRY in stabilizing the signalplex components at the rhabdomeres.


After maltose and glucose are exported to the cytosol, enzymes must exist to convert them to the precursors for sucrose synthesis. It was proposed that maltose metabolism in the cytosol of the plant cell is similar to that in the cytoplasm of Escherichia coli(Fig. 2) ( Boos & Shuman 1998 Lu & Sharkey 2004 ). In the cytoplasm of E. coli, maltose and maltodextrins of up to seven glucosyl residues are metabolized to G1P and G6P by the action of amylomaltase (MalQ), maltodextrin phosphorylase (MalP) and glucokinase ( Boos & Shuman 1998 ). It was reported by two different groups that cytosolic D-enzyme (DPE2) is involved in the conversion of maltose to sucrose ( Chia et al. 2004 Lu & Sharkey 2004 ). Cytosolic α-glucan phosphorylase (Pho2) was also suggested to be involved in maltose metabolism by its interaction with a heteroglycan in the cytosol ( Lu & Sharkey 2004 ). As the analogue of glucokinase in E. coli, hexokinase can convert glucose exported by the glucose transporter (pGlcT, At5g16150) and glucose produced by DPE2 to G6P (Fig. 2) ( Weber et al. 2000 Moore et al. 2003 Lu & Sharkey 2004 ). This may provide a mechanism for hexokinase to sense the carbon flux during starch degradation and to alter starch/sucrose ratio ( Sharkey et al. 2004a ). It should be noted that the subcellular localization of hexokinase in different species is different. Hexokinase in pea and spinach was located in the outer envelope of plastids ( Stitt et al. 1978 Wiese et al. 1999 ). Arabidopsis Hexokinase 1 (AtHXK1) was reported to be associated with the nuclear and cytosolic compartments of maize protoplasts ( Yanagisawa, Yoo & Sheen 2003 ). AtHXK1 was also shown to be associated with mitochondria (Balasubramanian, Karve, Kandasamy, Meagher & Moore, abstract submitted at the 16th International Conference on Arabidopsis Research, Madison, WI, USA). Although hexokinase might be attached to the outer membrane of different organelles, hexokinase is in close contact with the cytoplasm and is involved in cytosolic glycan metabolism. A comparison of maltose/maltodextrin metabolism in the cytoplasm of E. coli with maltose/heteroglycan metabolism in the cytosol of Arabidopsis leaves is shown in Fig. 2.

Comparison of maltose/maltodextrin metabolism in Escherichia coli with maltose/heteroglycan metabolism in Arabidopsis. F6P, fructose 6-phosphate G1P, glucose 1-phosphate G6P, glucose 6-phosphate MalQ, amylomaltase MalP, maltodextrin phosphorylase DPE2, disproportionating enzyme 2 Pi, orthophosphate Pho2, cytosolic α-glucan phosphorylase UDPG, uridine 5′-diphosphate glucose UTP, uridine 5′-triphosphate.

Cytosolic D-enzyme – activity with maltose?

Cytosolic D-enzyme (DPE2) and cytosolic α-glucan phosphorylase (Pho2) were found in the leaves of spinach, pea, Arabidopsis and potato (Fig. 1) ( Steup & Latzko 1979 Preiss, Okita & Greenberg 1980 Steup, Schachtele & Latzko 1980 Mori, Tanizawa & Fukui 1991 Duwenig et al. 1997 Chia et al. 2004 Lloyd et al. 2004 Lu & Sharkey 2004 ). These enzymes were considered to be starch-mobilizing enzymes and their presence in the cytosol was puzzling because there is no starch in the cytosol. Mutants of E. coli lacking MalQ accumulate maltose just like mutants of Arabidopsis lacking DPE2 ( Szmelcman et al. 1976 Lu & Sharkey 2004 ). Phylogenetic trees based on the protein sequences showed that DPE2 in Arabidopsis and rice is more closely related to MalQ in E. coli than to DPE1 in plants ( Lu & Sharkey 2004 ). Therefore, it was suggested that DPE2 is involved in maltose metabolism in the cytosol, analogous to the MalQ in E. coli (Fig. 2). We speculate that DPE2 acts on a highly branched heteroglycan in the cytosol and releases glucose from the reducing end, forms a heteroglycan-enzyme complex and transfers the heteroglycan to the non-reducing end of maltose. A similar mechanism in E. coli was proposed by Boos & Shuman (1998 ). Enzymatic activity of DPE2 with maltose was demonstrated by native glycogen gels ( Chia et al. 2004 ). Compared with the migration rate of DPE1 on native glycogen gels, DPE2 has a relatively higher affinity towards oyster glycogen, a polysaccharide with a degree of branching similar to the heteroglycan ( Chia et al. 2004 ). Protein domain prediction with Pfam indicated that DPE2 has a polysaccharide-binding domain located at the C-terminal of the protein sequence ( Bateman et al. 2004 ). The highest activity of recombinant DPE2 protein was recently found with glycogen or heteroglycan together with maltose (Lu, Steichen, Yao & Sharkey, unpublished results).

Nature of the cytosolic heteroglycan

In the cytosol of spinach, pea, Arabidopsis and potato leaves, there is a highly branched, water-soluble ethanol/KCl-insoluble heteroglycan (SHG), which has a high affinity towards cytosolic α-glucan phosphorylase (Pho2 or AtPHS2) ( Yang & Steup 1990 Fettke et al. 2004, 2005a, b Lu & Sharkey 2004 ). This heteroglycan mainly contains arabinose, galactose and glucose glucose in the heteroglycan only accounts for ≈ 5% of total monosaccharide content ( Yang & Steup 1990 Fettke et al. 2004, 2005a Lu & Sharkey 2004 ). It is plausible to speculate that the glucan residues in the heteroglycan, analogous to maltodextrin in the cytoplasm of E. coli, are both the substrate/product of DPE2 and the substrate for Pho2 in the cytosol (Fig. 1). This heteroglycan may also act as an overflow for carbohydrates formed from starch degradation at night when the production of hexoses exceeds the demand for and transport of sucrose, although the amount of the heteroglycan is substantially lower compared to the amount of starch in the leaf ( Lu & Sharkey 2004 ).

Cytosolic ‘starch’ phosphorylase

The involvement of Pho2 in transitory starch degradation is not clear. Antisense inhibition of Pho2 in potato plants has little impact on carbohydrate metabolism and it was proposed that Pho2 is not involved in starch degradation ( Duwenig et al. 1997 ). Because the maltose level and the hexose phosphate level in the chloroplast and cytosolic compartments of Pho2 RNAi potato plants were not measured ( Duwenig et al. 1997 ), we cannot rule out the possibility that Pho2 is involved in cytosolic glucan metabolism. Lu & Sharkey (2004 ) proposed that Pho2 phosphorylates glucan residues in heteroglycan and yields G1P, analogous to MalP in E. coli (Fig. 2). The interaction of Pho2 with the cytosolic heteroglycan (SHG) has been reported in spinach, pea and Arabidopsis ( Yang & Steup 1990 Fettke et al. 2004, 2005a ). In the presence of orthophosphate (Pi), SHG is used by Pho2 as a glucosyl donor, in the presence of G1P, SHG is used by Pho2 as a glucosyl acceptor ( Fettke et al. 2004 ). This suggests that Pho2 catalyses a bidirectional reaction and that the ratio of Pi/G1P in the cytosol determines the direction of the reaction. In the dark, cytosolic Pi concentration is about 700 nmol mg −1 Chl in the leaves of bean plants ( Sharkey & Vanderveer 1989 ). During the day, cytosolic G6P concentration is 54 nmol mg −1 Chl in the leaves of potato plants ( Sharkey & Vassey 1989 ). Because the G1P level is about one-fifth or less of the G6P level in the cytosol and night-time G1P level is not significantly different from daytime G1P level ( Lu et al. 2005 ), we estimate that there is much more Pi than G1P in the cytosol at night. This suggests that in vivo, Pho2 converts glucosyl residues in heteroglycan to G1P. A Pho2-deficient mutant of Arabidopsis had relatively higher amount of maltose at night, indicating that Pho2 is indeed involved in the cytosolic metabolism of maltose (Lu, Steichen, Yao & Sharkey, unpublished results).

Cytosolic α-glucosidase

α-Glucosidase hydrolyses maltose and maltodextrin to glucose. The occurrence and subcellular localization of α-glucosidase in the literature is conflicting. It was reported earlier that α-glucosidase activity was not detected in the leaves of pea and spinach ( Okita et al. 1979 Kruger & ap Rees 1983 Kakefuda, Duke & Hostak 1986 ). Years later, two apoplastic and one chloroplastic isoform were identified in pea seedlings, and the authors suggested inappropriate extraction and assays conditions might have caused non-detectable activity in their earlier studies ( Beers, Duke & Henson 1990 ). In the Arabidopsis genome, there are five genes encoding α-glucosidase-like proteins ( Smith et al. 2004 ). Among the five isozymes, At3g23640 is predicted to be cytosolic. If At3g23640 turns out to be a functional enzyme in the cytosol, the substantial increase in the maltose content in DPE2-deficient mutants indicates that the cytosolic α-glucosidase does not act on maltose. However, we cannot rule out the possibility that the cytosolic α-glucosidase acts on the heteroglycan to yield glucose. Glucose produced by α-glucosidase (or heteroglycan glucosidase 1, HGL1) can be converted to G6P by hexokinase (Fig. 1). Compared with the reaction catalysed by heteroglycan glucosidase, the reaction catalysed by α-glucan phosphorylase is preferred because hexokinase uses ATP to convert glucose to G6P, while α-glucan phosphorylase uses free phosphate to make G1P (Fig. 1). The binding of α-glucan phosphorylase to the SHG may help ensure that the energetically more efficient phosphorolytic path normally predominates.

18.6 Angiosperms

The flowering plants, also known as Angiospermae, or Magnoliophyta, are the most diverse group of land plants, with 64 orders, 416 families, approximately 13,000 known genera and 300,000 known species. Like gymnosperms, angiosperms are seed-producing plants. They are distinguished from gymnosperms by characteristics including flowers, endosperm within the seeds, and the production of fruits that contain the seeds. Etymologically, angiosperm means a plant that produces seeds within an enclosure in other words, a fruiting plant. The term comes from the Greek words angeion (“case” or “casing”) and sperma (“seed”).

Figure 18.8: Flowers of different families: St Bernards Lilly (Anthericum liliago): Liliaceae Bermuda Buttercup (Oxalis pescaprae): Oxalidaceae Oleander (Nerium oleander): Apocynaceae Lantana (Lantana camara): Verbenaceae Scarlet Pimpernel (Anagallis arvensis): Primulaceae Verbascum (Verbascum sinuatum): Scrophulariaceae Common Mallow (Malva sylvestris): Malvaceae Spanish Oyster (Scolymus hispanicus): Asteraceae Stork’s Bill (Erodium malacoides): Geraniaceae Bindweed (Convolvulus arvensis): Convolvulaceae Blue Gem (Hebe x franciscana): Plantaginaceae Calla Lily (Zantedeschia aethiopica): Araceae

The ancestors of flowering plants diverged from gymnosperms in the Triassic Period, 245 to 202 million years ago (mya), and the first flowering plants are known from

140 mya. They diversified extensively during the Early Cretaceous, became widespread by 120 mya, and replaced conifers as the dominant trees from 100 to 60 mya.

Angiosperms differ from other seed plants in several ways, described in the table below. These distinguishing characteristics taken together have made the angiosperms the most diverse and numerous land plants and the most commercially important group to humans.

Table 18.2: Distinctive features of angiosperms.
Feature Description
Flowering organs Flowers, the reproductive organs of flowering plants, are the most remarkable feature distinguishing them from the other seed plants. Flowers provided angiosperms with the means to have a more species-specific breeding system, and hence a way to evolve more readily into different species without the risk of crossing back with related species. Faster speciation enabled the Angiosperms to adapt to a wider range of ecological niches. This has allowed flowering plants to largely dominate terrestrialecosystems.[citation needed]
Stamens with two pairs of pollen sacs Stamens are much lighter than the corresponding organs of gymnosperms and have contributed to the diversification of angiosperms through time with adaptations to specialized pollination syndromes, such as particular pollinators. Stamens have also become modified through time to prevent self-fertilization, which has permitted further diversification, allowing angiosperms eventually to fill more niches.
Reduced male parts, three cells The male gametophyte in angiosperms is significantly reduced in size compared to those of gymnosperm seed plants. The smaller size of the pollen reduces the amount of time between pollination — the pollen grain reaching the female plant — and fertilization. In gymnosperms, fertilization can occur up to a year after pollination, whereas in angiosperms, fertilization begins very soon after pollination. The shorter amount of time between pollination and fertilization allows angiosperms to produce seeds earlier after pollination than gymnosperms, providing angiosperms a distinct evolutionary advantage.
Closed carpelenclosing the ovules (carpel or carpels and accessory parts may become the fruit) The closed carpel of angiosperms also allows adaptations to specialized pollination syndromes and controls. This helps to prevent self-fertilization, thereby maintaining increased diversity. Once the ovary is fertilized, the carpel and some surrounding tissues develop into a fruit. This fruit often serves as an attractant to seed-dispersing animals. The resulting cooperative relationship presents another advantage to angiosperms in the process of dispersal.
Reduced female gametophyte, seven cells with eight nuclei The reduced female gametophyte, like the reduced male gametophyte, may be an adaptation allowing for more rapid seed set, eventually leading to such flowering plant adaptations as annual herbaceous life-cycles, allowing the flowering plants to fill even more niches.
Endosperm In general, endosperm formation begins after fertilization and before the first division of the zygote. Endosperm is a highly nutritive tissue that can provide food for the developing embryo, the cotyledons, and sometimes the seedling when it first appears.

Angiosperm stems are made up of seven layers as shown on the right. The amount and complexity of tissue-formation in flowering plants exceeds that of gymnosperms. The vascular bundles of the stem are arranged such that the xylem and phloem form concentric rings.

In the dicotyledons, the bundles in the very young stem are arranged in an open ring, separating a central pith from an outer cortex. In each bundle, separating the xylem and phloem, is a layer of meristem or active formative tissue known as cambium. By the formation of a layer of cambium between the bundles (interfascicular cambium), a complete ring is formed, and a regular periodical increase in thickness results from the development of xylem on the inside and phloem on the outside. The soft phloem becomes crushed, but the hard wood persists and forms the bulk of the stem and branches of the woody perennial. Owing to differences in the character of the elements produced at the beginning and end of the season, the wood is marked out in transverse section into concentric rings, one for each season of growth, called annual rings.

Among the monocotyledons, the bundles are more numerous in the young stem and are scattered through the ground tissue. They contain no cambium and once formed the stem increases in diameter only in exceptional cases.

The characteristic feature of angiosperms is the flower. Flowers show remarkable variation in form and elaboration, and provide the most trustworthy external characteristics for establishing relationships among angiosperm species. The function of the flower is to ensure fertilization of the ovule and development of fruit containing seeds. The floral apparatus may arise terminally on a shoot or from the axil of a leaf (where the petiole attaches to the stem). Occasionally, as in violets, a flower arises singly in the axil of an ordinary foliage-leaf. More typically, the flower-bearing portion of the plant is sharply distinguished from the foliage-bearing or vegetative portion, and forms a more or less elaborate branch-system called an inflorescence.

Figure 18.10: Reproductive parts of Easter Lily (Lilium longiflorum).1. Stigma, 2. Style, 3. Stamens, 4. Filament, 5. Petal

There are two kinds of reproductive cells produced by flowers. Microspores, which will divide to become pollen grains, are the “male” cells and are borne in the stamens (or microsporophylls). The “female” cells called megaspores, which will divide to become the egg cell (megagametogenesis), are contained in the ovule and enclosed in the carpel (or megasporophyll).

The flower may consist only of these parts, as in willow, where each flower comprises only a few stamens or two carpels. Usually, other structures are present and serve to protect the sporophylls and to form an envelope attractive to pollinators. The individual members of these surrounding structures are known as sepals and petals (or tepals in flowers such as Magnolia where sepals and petals are not distinguishable from each other). The outer series (calyx of sepals) is usually green and leaf-like, and functions to protect the rest of the flower, especially the bud. The inner series (corolla of petals) is, in general, white or brightly colored, and is more delicate in structure. It functions to attract insect or bird pollinators. Attraction is effected by color, scent, and nectar, which may be secreted in some part of the flower. The characteristics that attract pollinators account for the popularity of flowers and flowering plants among humans.

While the majority of flowers are perfect or hermaphrodite (having both pollen and ovule producing parts in the same flower structure), flowering plants have developed numerous morphological and physiological mechanisms to reduce or prevent self-fertilization. Heteromorphic flowers have short carpels and long stamens, or vice versa, so animal pollinators cannot easily transfer pollen to the pistil (receptive part of the carpel). Homomorphic flowers may employ a biochemical (physiological) mechanism called self-incompatibility to discriminate between self and non-self pollen grains. In other species, the male and female parts are morphologically separated, developing on different flowers.

The botanical term “Angiosperm”, from the Ancient Greek ἀγγεῖον, angeíon (bottle, vessel) and σπέρμα, sperma (seed), was coined in the form Angiospermae by Paul Hermann in 1690, as the name of one of his primary divisions of the plant kingdom. This included flowering plants possessing seeds enclosed in capsules, distinguished from his Gymnospermae, or flowering plants with achenial or schizo-carpic fruits, the whole fruit or each of its pieces being here regarded as a seed and naked. The term and its antonym were maintained by Carl Linnaeus with the same sense, but with restricted application, in the names of the orders of his class Didynamia. Its use with any approach to its modern scope became possible only after 1827, when Robert Brown established the existence of truly naked ovules in the Cycadeae and Coniferae, and applied to them the name Gymnosperms. From that time onward, as long as these Gymnosperms were, as was usual, reckoned as dicotyledonous flowering plants, the term Angiosperm was used antithetically by botanical writers, with varying scope, as a group-name for other dicotyledonous plants.

In 1851, Hofmeister discovered the changes occurring in the embryo-sac of flowering plants, and determined the correct relationships of these to the Cryptogamia. This fixed the position of Gymnosperms as a class distinct from Dicotyledons, and the term Angiosperm then gradually came to be accepted as the suitable designation for the whole of the flowering plants other than Gymnosperms, including the classes of Dicotyledons and Monocotyledons. This is the sense in which the term is used today.

In most taxonomies, the flowering plants are treated as a coherent group. The most popular descriptive name has been Angiospermae (Angiosperms), with Anthophyta (“flowering plants”) a second choice. These names are not linked to any rank. The Wettstein system and the Engler system use the name Angiospermae, at the assigned rank of subdivision. The Reveal system treated flowering plants as subdivision Magnoliophytina, but later split it to Magnoliopsida, Liliopsida, and Rosopsida. The Takhtajan system and Cronquist system treat this group at the rank of division, leading to the name Magnoliophyta (from the family name Magnoliaceae). The Dahlgren system and Thorne system (1992) treat this group at the rank of class, leading to the name Magnoliopsida. The APG system of 1998, and the later 2003 and 2009 revisions, treat the flowering plants as a clade called angiosperms without a formal botanical name. A formal classification was published alongside the 2009 revision in which the flowering plants form the Subclass Magnoliidae.

The internal classification of this group has undergone considerable revision. The Cronquist system, proposed by Arthur Cronquist in 1968 and published in its full form in 1981, is still widely used but is no longer believed to accurately reflect phylogeny. A consensus about how the flowering plants should be arranged has recently begun to emerge through the work of the Angiosperm Phylogeny Group (APG), which published an influential reclassification of the angiosperms in 1998. Updates incorporating more recent research were published as the APG II system in 2003, the APG III system in 2009, and the APG IV system in 2016.

Traditionally, the flowering plants are divided into two groups,

which in the Cronquist system are called Magnoliopsida (at the rank of class, formed from the family name Magnoliaceae) and Liliopsida (at the rank of class, formed from the family name Liliaceae). Other descriptive names allowed by Article 16 of the ICBN include Dicotyledones or Dicotyledoneae, and Monocotyledones or Monocotyledoneae, which have a long history of use. In English a member of either group may be called a dicotyledon (plural dicotyledons) and monocotyledon (plural monocotyledons), or abbreviated, as dicot (plural dicots) and monocot (plural monocots). These names derive from the observation that the dicots most often have two cotyledons, or embryonic leaves, within each seed. The monocots usually have only one, but the rule is not absolute either way. From a broad diagnostic point of view, the number of cotyledons is neither a particularly handy, nor a reliable character.

Recent studies, as by the APG, show that the monocots form a monophyletic group (clade) but that the dicots do not (they are paraphyletic). Nevertheless, the majority of dicot species do form a monophyletic group, called the eudicots or tricolpates. Of the remaining dicot species, most belong to a third major clade known as the magnoliids, containing about 9,000 species. The rest include a paraphyletic grouping of early branching taxa known collectively as the basal angiosperms, plus the families Ceratophyllaceae and Chloranthaceae.

Fossilized spores suggest that land plants (embryophytes) have existed for at least 475 million years. Early land plants reproduced sexually with flagellated, swimming sperm, like the green algae from which they evolved. An adaptation to terrestrialization was the development of upright meiosporangia for dispersal by spores to new habitats. This feature is lacking in the descendants of their nearest algal relatives, the Charophycean green algae. A later terrestrial adaptation took place with retention of the delicate, avascular sexual stage, the gametophyte, within the tissues of the vascular sporophyte. This occurred by spore germination within sporangia rather than spore release, as in non-seed plants. A current example of how this might have happened can be seen in the precocious spore germination in Selaginella, the spike-moss. The result for the ancestors of angiosperms was enclosing them in a case, the seed.

The apparently sudden appearance of nearly modern flowers in the fossil record initially posed such a problem for the theory of evolution that Charles Darwin called it an “abominable mystery”. However, the fossil record has considerably grown since the time of Darwin, and recently discovered angiosperm fossils such as Archaefructus, along with further discoveries of fossil gymnosperms, suggest how angiosperm characteristics may have been acquired in a series of steps. Several groups of extinct gymnosperms, in particular seed ferns, have been proposed as the ancestors of flowering plants, but there is no continuous fossil evidence showing exactly how flowers evolved. Some older fossils, such as the upper Triassic Sanmiguelia, have been suggested.

Figure 18.11: A Bee orchid has evolved over many generations to better mimic a female bee to attract male bees as pollinators.

The first seed bearing plants, like the ginkgo, and conifers (such as pines and firs), did not produce flowers. The pollen grains (male gametophytes) of Ginkgo and cycads produce a pair of flagellated, mobile sperm cells that “swim” down the developing pollen tube to the female and her eggs.

Oleanane, a secondary metabolite produced by many flowering plants, has been found in Permian deposits of that age together with fossils of gigantopterids. Gigantopterids are a group of extinct seed plants that share many morphological traits with flowering plants, although they are not known to have been flowering plants themselves.

Based on current evidence, some propose that the ancestors of the angiosperms diverged from an unknown group of gymnosperms in the Triassic period (245–202 million years ago). Fossil angiosperm-like pollen from the Middle Triassic (247.2–242.0 Ma) suggests an older date for their origin. A close relationship between angiosperms and gnetophytes, proposed on the basis of morphological evidence, has more recently been disputed on the basis of molecular evidence that suggest gnetophytes are instead more closely related to other gymnosperms.

The fossil plant species Nanjinganthus dendrostyla from Early Jurassic China seems to share many exclusively angiosperm features, such as a thickened receptacle with ovules, and thus might represent a crown-group or a stem-group angiosperm. However, the interpretation of the structures in this fossils are highly contested.

The evolution of seed plants and later angiosperms appears to be the result of two distinct rounds of whole genome duplication events. These occurred at 319 million years ago and 192 million years ago. Another possible whole genome duplication event at 160 million years ago perhaps created the ancestral line that led to all modern flowering plants. That event was studied by sequencing the genome of an ancient flowering plant, Amborella trichopoda, and directly addresses Darwin’s “abominable mystery”.

One study has suggested that the early-middle Jurassic plant Schmeissneria, traditionally considered a type of ginkgo, may be the earliest known angiosperm, or at least a close relative.

It has been proposed that the swift rise of angiosperms to dominance was facilitated by a reduction in their genome size. During the early Cretaceous period, only angiosperms underwent rapid genome downsizing, while genome sizes of ferns and gymnosperms remained unchanged. Smaller genomes—and smaller nuclei—allow for faster rates of cell division and smaller cells. Thus, species with smaller genomes can pack more, smaller cells—in particular veins and stomata—into a given leaf volume. Genome downsizing therefore facilitated higher rates of leaf gas exchange (transpiration and photosynthesis) and faster rates of growth. This would have countered some of the negative physiological effects of genome duplications, facilitated increased uptake of carbon dioxide despite concurrent declines in atmospheric CO2) concentrations, and allowed the flowering plants to outcompete other land plants.

The earliest known macrofossil confidently identified as an angiosperm, Archaefructus liaoningensis, is dated to about 125 million years BP (the Cretaceous period), whereas pollen considered to be of angiosperm origin takes the fossil record back to about 130 million years BP, with Montsechia representing the earliest flower at that time. In 2018, scientists reported that the earliest flowers began about 180 million years ago, 50 million years earlier than thought earlier. Nonetheless, circumstantial chemical evidence has been found for the existence of angiosperms as early as 250 million years ago .

In 2013 flowers encased in amber were found and dated 100 million years before present. The amber had frozen the act of sexual reproduction in the process of taking place. Microscopic images showed tubes growing out of pollen and penetrating the flower’s stigma. The pollen was sticky, suggesting it was carried by insects. In August 2017, scientists presented a detailed description and 3D model image of what the first flower possibly looked like, and presented the hypothesis that it may have lived about 140 million years ago. A Bayesian analysis of 52 angiosperm taxa suggested that the crown group of angiosperms evolved between 178 million years ago and 198 million years ago.

Recent DNA analysis based on molecular systematics showed that Amborella trichopoda, found on the Pacific island of New Caledonia, belongs to a sister group of the other flowering plants, and morphological studies suggest that it has features that may have been characteristic of the earliest flowering plants. The orders Amborellales, Nymphaeales, and Austrobaileyales diverged as separate lineages from the remaining angiosperm clade at a very early stage in flowering plant evolution.

The great angiosperm radiation, when a great diversity of angiosperms appears in the fossil record, occurred in the mid-Cretaceous (approximately 100 million years ago). However, a study in 2007 estimated that the division of the five most recent (the genus Ceratophyllum, the family Chloranthaceae, the eudicots, the magnoliids, and the monocots) of the eight main groups occurred around 140 million years ago. It is generally assumed that the function of flowers, from the start, was to involve mobile animals in their reproduction processes. That is, pollen can be scattered even if the flower is not brightly colored or oddly shaped in a way that attracts animals however, by expending the energy required to create such traits, angiosperms can enlist the aid of animals and, thus, reproduce more efficiently.

Island genetics provides one proposed explanation for the sudden, fully developed appearance of flowering plants. Island genetics is believed to be a common source of speciation in general, especially when it comes to radical adaptations that seem to have required inferior transitional forms. Flowering plants may have evolved in an isolated setting like an island or island chain, where the plants bearing them were able to develop a highly specialized relationship with some specific animal (a wasp, for example). Such a relationship, with a hypothetical wasp carrying pollen from one plant to another much the way fig wasps do today, could result in the development of a high degree of specialization in both the plant(s) and their partners. Note that the wasp example is not incidental bees, which, it is postulated, evolved specifically due to mutualistic plant relationships, are descended from wasps.

Animals are also involved in the distribution of seeds. Fruit, which is formed by the enlargement of flower parts, is frequently a seed-dispersal tool that attracts animals to eat or otherwise disturb it, incidentally scattering the seeds it contains (see frugivory). Although many such mutualistic relationships remain too fragile to survive competition and to spread widely, flowering proved to be an unusually effective means of reproduction, spreading (whatever its origin) to become the dominant form of land plant life.

Flower ontogeny uses a combination of genes normally responsible for forming new shoots. The most primitive flowers probably had a variable number of flower parts, often separate from (but in contact with) each other. The flowers tended to grow in a spiral pattern, to be bisexual (in plants, this means both male and female parts on the same flower), and to be dominated by the ovary (female part). As flowers evolved, some variations developed parts fused together, with a much more specific number and design, and with either specific sexes per flower or plant or at least “ovary-inferior”. Flower evolution continues to the present day modern flowers have been so profoundly influenced by humans that some of them cannot be pollinated in nature. Many modern domesticated flower species were formerly simple weeds, which sprouted only when the ground was disturbed. Some of them tended to grow with human crops, perhaps already having symbiotic companion plant relationships with them, and the prettiest did not get plucked because of their beauty, developing a dependence upon and special adaptation to human affection.

A few paleontologists have also proposed that flowering plants, or angiosperms, might have evolved due to interactions with dinosaurs. One of the idea’s strongest proponents is Robert T. Bakker. He proposes that herbivorous dinosaurs, with their eating habits, provided a selective pressure on plants, for which adaptations either succeeded in deterring or coping with predation by herbivores.

By the late Cretaceous, angiosperms appear to have dominated environments formerly occupied by ferns and cycadophytes, but large canopy-forming trees replaced conifers as the dominant trees only close to the end of the Cretaceous 66 million years ago or even later, at the beginning of the Tertiary. The radiation of herbaceous angiosperms occurred much later. Yet, many fossil plants recognizable as belonging to modern families (including beech, oak, maple, and magnolia) had already appeared by the late Cretaceous. Flowering plants appeared in Australia about 126 million years ago. This also pushed the age of ancient Australian vertebrates, in what was then a south polar continent, to 126-110 million years old.

18.6.1 Fertilization and Embryogenesis

Double fertilization refers to a process in which two sperm cells fertilize cells in the ovule. This process begins when a pollen grain adheres to the stigma of the pistil (female reproductive structure), germinates, and grows a long pollen tube. While this pollen tube is growing, a haploid generative cell travels down the tube behind the tube nucleus. The generative cell divides by mitosis to produce two haploid (n) sperm cells. As the pollen tube grows, it makes its way from the stigma, down the style and into the ovary. Here the pollen tube reaches the micropyle of the ovule and digests its way into one of the synergids, releasing its contents (which include the sperm cells). The synergid that the cells were released into degenerates and one sperm makes its way to fertilize the egg cell, producing a diploid (2n) zygote. The second sperm cell fuses with both central cell nuclei, producing a triploid (3n) cell. As the zygote develops into an embryo, the triploid cell develops into the endosperm, which serves as the embryo’s food supply. The ovary will now develop into a fruit and the ovule will develop into a seed.

As the development of embryo and endosperm proceeds within the embryo sac, the sac wall enlarges and combines with the nucellus (which is likewise enlarging) and the integument to form the seed coat. The ovary wall develops to form the fruit or pericarp, whose form is closely associated with type of seed dispersal system.

Frequently, the influence of fertilization is felt beyond the ovary, and other parts of the flower take part in the formation of the fruit, e.g., the floral receptacle in the apple, strawberry, and others.

The character of the seed coat bears a definite relation to that of the fruit. They protect the embryo and aid in dissemination they may also directly promote germination. Among plants with indehiscent fruits, in general, the fruit provides protection for the embryo and secures dissemination. In this case, the seed coat is only slightly developed. If the fruit is dehiscent and the seed is exposed, in general, the seed-coat is well developed, and must discharge the functions otherwise executed by the fruit.

Flowering plants generate gametes using a specialized cell division called meiosis. Meiosis takes place in the ovule (a structure within the ovary that is located within the pistil at the center of the flower) (see diagram labeled “Angiosperm lifecycle”). A diploid cell (megaspore mother cell) in the ovule undergoes meiosis (involving two successive cell divisions) to produce four cells (megaspores) with haploid nuclei. It is thought that the basal chromosome number in angiosperms is n = 7. One of these four cells (megaspore) then undergoes three successive mitotic divisions to produce an immature embryo sac (megagametophyte) with eight haploid nuclei. Next, these nuclei are segregated into separate cells by cytokinesis to producing 3 antipodal cells, 2 synergid cells and an egg cell. Two polar nuclei are left in the central cell of the embryo sac.

Pollen is also produced by meiosis in the male anther (microsporangium). During meiosis, a diploid microspore mother cell undergoes two successive meiotic divisions to produce 4 haploid cells (microspores or male gametes). Each of these microspores, after further mitoses, becomes a pollen grain (microgametophyte) containing two haploid generative (sperm) cells and a tube nucleus. When a pollen grain makes contact with the female stigma, the pollen grain forms a pollen tube that grows down the style into the ovary. In the act of fertilization, a male sperm nucleus fuses with the female egg nucleus to form a diploid zygote that can then develop into an embryo within the newly forming seed. Upon germination of the seed, a new plant can grow and mature.

Figure 18.12: Scanning electron microscope image (500x magnification) of pollen grains from a variety of common plants: sunflower (Helianthus annuus), morning glory (Ipomoea purpurea), prairie hollyhock (Sidalcea malviflora), oriental lily (Lilium auratum), evening primrose (Oenothera fruticosa), and castor bean (Ricinus communis).The image is magnified some x500, so the bean shaped grain in the bottom left corner is about 50 μm long. The colors are computer-generated.

The adaptive function of meiosis is currently a matter of debate. A key event during meiosis in a diploid cell is the pairing of homologous chromosomes and homologous recombination (the exchange of genetic information) between homologous chromosomes. This process promotes the production of increased genetic diversity among progeny and the recombinational repair of damages in the DNA to be passed on to progeny. To explain the adaptive function of meiosis in flowering plants, some authors emphasize diversity and others emphasize DNA repair.


Flowering is the developmental transition from vegetative growth to reproductive growth during the plant life cycle. In Arabidopsis, the time of flowering is regulated by several pathways, including the autonomous, vernalization and photoperiod pathways (Simpson and Dean, 2002 Imaizumi and Kay, 2006 Amasino, 2010 ). The autonomous pathway senses endogenous signals rather than environmental cues the vernalization pathway can accelerate flowering after the plants undergo a prolonged period of cold (e.g. winter). These two pathways are integrated and together repress the transcription of the central flowering repressor gene FLC (Michaels and Amasino, 2001 Putterill et al., 2004 ). The photoperiod pathway can sense day length the core mechanism of this pathway is the circadian regulation of the degradation of CONSTANS (CO), a major flowering promoter (Valverde et al., 2004 Imaizumi et al., 2005 ). In long-day conditions (LD), the protein level of CO reaches its peak at dusk, and is then degraded throughout the night, facilitating the expression of floral integrator genes in short-day conditions (SD), the protein level of CO is low and does not have major effects on floral integrator genes, resulting in delayed flowering (Samach et al., 2000 Suarez-Lopez et al., 2001 Yanovsky and Kay, 2002 ). Mutations in components of the photoperiod pathway result in delayed flowering in LD but do not affect flowering time in SD (Koornneef et al., 1991 Song et al., 2012 ). The convergence of the aforementioned three flowering pathways results in activation of the floral integrator genes, FT, SOC1 and LFY. This activation then upregulates the expression of floral identity genes, ultimately stimulating flowering.

Histone modifications including methylation, acetylation, ubiquitination and phosphorylation are all known to be involved in regulating the expression of flowering regulatory genes in Arabidopsis (He and Amasino, 2005 Li et al., 2007 He, 2012 Su et al., 2017 ). Histone acetylation, which is correlated with transcriptional activation, is added by histone acetyltransferases and is removed by histone deacetylases (HDACs). In Arabidopsis, the conserved RPD3-like HDACs consist of 12 putative members (Pandey et al., 2002 Hollender and Liu, 2008 Peng et al., 2017 ), in which HDA5, HDA6, HDA9 and HDA19 have been well studied. HDA5 promotes flowering time by repressing the expression of the flowering repressor genes FLC and MAF1 (Luo et al., 2015 ). HDA9 is involved in the regulation of both leaf senescence and flowering time (Kang et al., 2015 Chen et al., 2016 Kim et al., 2016 ). HDA9 delays flowering time by repressing the expression of AGL19 and thus promoting the expression of FT especially in SD (Kang et al., 2015 Kim et al., 2016 ). HDA6 is required for DNA methylation and heterochromatin silencing (Murfett et al., 2001 Aufsatz et al., 2002 Gu et al., 2011 Pontvianne et al., 2013 Yu et al., 2017 ). Moreover, HDA6 is involved in phytohormone signaling, circadian transcription, stress responses and the regulation of flowering time (Wu et al., 2008 Chen et al., 2010 Yu et al., 2011 Zhu et al., 2011 Wang et al., 2013 Kim et al., 2017 ). In the hda6 mutant, the FLC expression is de-repressed, and flowering time is delayed under both LD and SD double-mutant analysis has shown that the delayed flowering time phenotype of the hda6 mutant can be restored to the wild-type level in plants that harbor both the hda6 and flc mutations (Wu et al., 2008 Yu et al., 2011 ). This finding clearly demonstrates that HDA6 represses the expression of FLC and thereby regulates flowering time. HDA19 functions either redundantly with, or independently of, HDA6 in various biological processes, including embryogenesis, germination, floral development, phytohormone signaling and stress responses (Tian et al., 2005 Zhou et al., 2005 Tanaka et al., 2008 Chen and Wu, 2010 Chen et al., 2010 Krogan et al., 2012 ). Whereas HDA6 is known to regulate flowering time via its repression of FLC expression, very little is known about the possible function of HDA19 in the regulation of flowering time.

In Arabidopsis, the SIN3-like proteins SNL1–SNL6, the RbAp48 homolog MSI1, and the Rxt3 homolog HDC1 have been shown to interact with HDA19 and/or HDA6 (Perrella et al., 2013 Wang et al., 2013 Mehdi et al., 2016 ). SNL3, also known as ATSIN3, participates in abscisic acid (ABA) responses by interacting with the APETALA2/EREBP-type transcription factor AtERF7 (Song et al., 2005 ). SNL1 and SNL2 regulate seed dormancy by decreasing histone acetylation of key genes involved in the ethylene and ABA signaling pathways (Wang et al., 2013 ). MSI1 is not only a subunit of the Arabidopsis RPD3 HDAC complex, but is also a subunit of the PRC2 histone H3K27 methyltransferase complex and the CAF1 chromatin assembly complex (Kaya et al., 2001 Kohler et al., 2003 Mehdi et al., 2016 ). Loss-of-function of MSI1 causes a late-flowering phenotype (Steinbach and Hennig, 2014 ). However, considering that MSI1 is known to be a component of at least three protein complexes, it is not yet known which complex is responsible for the role of MSI1 in the regulation of flowering time. HDC1 was shown to regulate flowering time, plant growth and ABA sensitivity, and the late-flowering phenotype of the hdc1 mutant was shown to be caused by de-repression of FLC (Perrella et al., 2013 ). Although both MSI1 and HDC1 are known to regulate flowering time, we do not know how these two subunits—both of which shared by the HDA6 and HDA19 HDAC complexes—are functionally coordinated to regulate flowering time.

Here, we demonstrate that HDA6 and HDA19 can independently interact with SIN3-like proteins (SNLs), with MSI1, and with HDC1, and thereby form RPD3-type HDAC complexes in Arabidopsis. While the hda6 mutant plants flower later than the wild-type plants in both LD and SD, the hdc1 mutant plants flower later than the wild-type in LD and flower earlier than the wild-type in SD. In LD, the late-flowering phenotype is dependent on FLC in the hda6 mutant but is independent of FLC in the hdc1 mutant. This observation contradicts a previous study that reported that the hdc1 mutant has increased FLC expression and thereby causes a late-flowering phenotype in LD (Perrella et al., 2013 ). Our results support a photoperiod-dependent role for HDC1 in the regulation of flowering time. HDC1 is a shared component of the HDA6 and HDA19 HDAC complexes, and its role in the photoperiod-dependent regulation of flowering time is shared by HDA19 and SNL2/3/4, but not by HDA6. Our study reveals that an epigenetic mechanism controls photoperiod-dependent flowering time, thus deepening our understanding of how chromatin modifications differentially regulate flowering time in response to photoperiodic signals.

Get out

Direct trains connect Amsterdam to Paris, to major Belgian cities like Brussels and Antwerp, and to German cities like Cologne, Frankfurt and Berlin. The ticket machines directly sell tickets to nearby destinations in Belgium and Germany, for longer journeys you will need to consult the international ticket office at the west end of the Central Station. CityNightLine trains run directly from Amsterdam Central Station to Milan, Vienna, Copenhagen, Prague, Warsaw, Moscow, Munich, Innsbruck, and Zurich (reservation compulsory).

Almost any place in the Netherlands can be reached within 3 hr of rail travel. To make more sense, day trips can be divided into those close to the city (about 30 min by public transport) and those further afield.

Watch the video: Lush Lilies. Urban Flower (July 2022).


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