Presented here is a simple teaching lab to illustrate the dynamic qualities of plant movement using smartphones to create movies of gravitropism and circumnutation. Within as little as 90 minutes, students can observe dramatic changes in plant position using the easy-to-grow, simple genetic model plant, Arabidopsis thaliana. Student assessment revealed that 64 percent of students stated that this lab increased their interest in plants; and interestingly, 46 percent of students showed their movies to individuals who were not associated with the teaching lab, strongly suggesting that this teaching method can be used to propagate interest in plants to individuals in society at large.

Introduction

Plant biology is considered one of the least interesting topics among undergraduate biology students, despite the fundamental role plants play in preserving the world's life system, providing food, materials for clothing, transportation, and housing. In one study of first year undergraduate biology majors, it was shown that among various topics of interests, plants rated lowest. On a scale ranging from zero to five, plants were given a favorable rating of 1.2, animals 3.3, and studies on the human body were rated at 4.3 (Marbach-Ad, 2004). This lack of interest in plants among undergraduates, and the world at large, has been diagnosed as “plant blindness,” a term coined by Wandersee and Schussler (1999) to describe students who are simply unaware of the importance of plants. Similar to this is “plant illiteracy” (Uno, 2009), characterized by students’ lack of knowledge regarding the importance of plants in society and agriculture. The root cause of plant blindness and illiteracy stems from the unfortunate fact that students are growing up in an increasingly technologized and urbanized society where they are disconnected from plants, and nature in general, a condition broadly known as nature deficit disorder (Louv, 2008).

Because plants are fundamental to life itself and provide resources necessary for survival, new teaching methods must be developed to enhance interest in plants for both conservation and agricultural reasons. A few contemporary examples to enhance student interest include providing direct access to living materials in botanical gardens (Nyberg & Sanders, 2014), delivering methods of digital visualization of histological slides (Bonser et al., 2013), and using the model molecular system Arabidopsis to teach contemporary plant research methods (Mulligan & Anderson, 1995). However, because these methods are static, students miss the more interesting aspects of plant behavior in that plants operate on a different time scale in which change is not easily perceived.

When examined through the lens of time, plants reveal a fascinating dynamic. In nature plants move to survive: leaves adjust their position to capture maximum light; whole shoots twist and turn to out-maneuver neighbors competing for light; parasitic plants stalk other plants; and root tips forage through the soil in search for nutrients. These dynamics can be shown by instructors using time-lapse movies (see Plant Movements Revealed [Stark, 2008], in which one can find an extensive list of time-lapse movies, including the popular Plants in Motion website [Hangarter, 2000]). Still, these methods are unidirectional from an educational perspective; it is little different than watching TV. A student is observing someone else's observations.

A more exciting and intimate way to study plants involves students creating time-lapse movies in the lab. To date, only two examples of comprehensive time-lapse teaching labs have been reported in the literature (Hangarter, 2000; Harrison-Pitaniello, 2013); these methods do not use smartphones or tablets, but instead a computer with a camcorder. With a smartphone or tablet, one simply records a video on the same device. The logical next step is for students to use their smart phones and tablets to enhance their understanding of plant movement.

Smartphone- and tablet-facilitated time-lapse investigations can now be conducted by students with ease. This follows a logical trend as smartphones and tablets are increasingly used in the classroom. As of 2013, over 87 percent of college students have a smartphone, and presumably the number is nearing 100 percent in the four years that have passed. The amount of time the average college student spends per day on their smartphone is 528 minutes—8.8 hours! (Roberts et al., 2014). Smartphones and tablets present an excellent tool to enhance students’ understanding of plant movement.

Plant Time-Lapse Topics: Gravitropism and Circumnutation

Gravitropism is a core concept taught in most standard undergraduate biology and upper level plant physiology lectures. Proper gravitropic responses enhance nutrient and light acquisition and are thus essential for plant survival. Because gravitropic movements are fast (relatively speaking), it is a phenomenon highly suitable to time-lapse studies during one classroom lab period (1½–3 hours).

Another “rapid” plant movement is circumnutation. Circumnutation is a universal but poorly understood plant movement that refers to the inherent back and forth rhythm and elaborate undulations of plant structures that occur in both roots and shoots (Stolarz, 2009). It involves a hydraulic mechanism that causes rotational waves around a collar of cells surrounding the central axis at the bending zone (Lubkin, 1994). Both gravitropism and circumnutation (and phototropism, as well) have been the subject of scientific study for over a century, and were a focus area of Darwin's investigations into plant movement (Darwin, 1880). The advent of personal time-lapse tools open up Darwin's work, as well as subsequent years of physiological and molecular studies on this subject, to student-led inquiry.

Here I present a constructivist, hands-on approach for students to reevaluate their misunderstanding of plants as static, uninteresting organisms. Students see firsthand how plants are continuous, moving organisms, and in doing so, perform studies to uncover the dynamic reality of plant movements using the simple genetic model, Arabidopsis, a “rapid” moving plant. The study itself runs from 1½ to 2½ hours (longer times are better).

The Principles of Biology (POB) Lab

POB laboratory is the introductory biology class on the natural basis of life. This course gives NYU students the intellectual and technical skills to understand modern biological investigative research. The POB lab mostly serves those on a premed track, but also students interested in other health-related careers, and a minority who will continue their studies in biological fields earning a master's degree or a PhD. This course typically has a large enrollment ranging from 360 to 500 students, depending on the year.

Arabidopsis is the Winner of the “Plant Derby”

To construct a time-lapse smartphone/tablet-driven lab, a variety of different plant species were recorded over a period of 2 hours and 45 minutes (the time span of the Introductory Biology Lab) to find a species that showed the fastest root bending. Sterile plants (Arabidopsis, Brassica, corn, and radish) were grown from seed using a nonasceptic method (Bargmann et al., 2014) on agar media with MS (Murashige & Skoog, 1962) salts, and were evaluated qualitatively for primary roots that showed the most obvious and rapid bending following a 90° change in orientation. The winner of this time-lapse plant derby turned out to be radish roots. Yet, when students viewed these movies of radish roots bending, they were not impressed. While contemplating a better system, I serendipitously found Arabidopsis shoots to be an ideal species/organ for developing a time-lapse teaching lab; I was growing the Arabidopsis seedlings on soil from the plant derby to produce seed, and on a lark, after about four weeks of growth, I placed the Arabidopsis plants on their side. Here I recorded a dramatic rapid reorientation of growth—a 90° upward turning movement of the stem inflorescence apex—using the free version of the program, Lapse It, available at lapseit.com.

During testing, when the Arabidopsis plants were turned 90° onto their side (Figure 1), inflorescence stems displayed rapid reorientation of the shoot apex to a vertical position within 90 minutes. The timing of this response agrees with published data (Fukaki et al., 1996). It was also noted that control plants (those kept upright) were circumnutating with the inflorescence apex moving with approximately one to two full nutations within the same time period (Figure 1). A useful advantage of Arabidopsis is the vast strain and mutant collection publicly available through the Arabidopsis Biological Resource Center (ABRC), which permits one to observe the affects of genetic variation on movement (Mulligan & Anderson, 1995). In addition, Arabidopsis is inexpensive and easy to grow and store, and is popular for teaching various topics in plant biology (Mulligan & Anderson, 1995).

Figure 1.
Simple laboratory set up for a time-lapse Arabidopsis movement assay. Both gravitropism (plant on left) and circumnutation (plant on right) are captured with an iPhone using the freely available LapseIt program.
Figure 1.
Simple laboratory set up for a time-lapse Arabidopsis movement assay. Both gravitropism (plant on left) and circumnutation (plant on right) are captured with an iPhone using the freely available LapseIt program.

Test Study: An Observational Time-Lapse Lab to Record Plant Movement in a Large Class Setting

A time-lapse exercise designed to create videos of Arabidopsis movement was tested Spring, 2015, in the POB Lab class. Here 425 students used personal smartphones/tablets to record four-week-old Arabidopsis shoots (inflorescence stems) either upright (control), or turned on their side (90°). Movies were recorded over a period of 2 hours to 2 hours 45 minutes using Lapse It.

Plant Culture Methods

Standard Arabidopsis cultivation methods were used (similar to Bargman et al., 2014). In this system Arabidopsis seeds were grown on MetroMix 360. A few seeds per pot were sprinkled over wet soil in 1½-inch square plastic pots that were arranged in rectangular rows sitting in plastic flats. After seeding, the flats were covered with a clear plastic top to keep humidity high during germination. (To enhance germination, pots with sown seeds can then be stored at 4°C for two to three days, as a stratification step to improve germination; however, we have found this is unnecessary when working with the Arabidopsis cultivar, Columbia, which germinated in our possession without stratification.) Approximately one week after germination, the plastic top was removed. During cultivation plants were bottom-watered: water was applied to the bottom of the flat so that the base of the plant pots were submerged and water moved into the soil through capillary action. The water in the flat was allowed to dry out in between waterings; however, the soil was never allowed to become completely dry (otherwise the plants may desiccate and die). After seeds had germinated a sprinkle of Miracle Grow Bloom Booster Flower Food fertilizer powder (NPK of 15-30-15, with the following microelements: B 0.02%, Cu 0.07%, Fe 0.15%, Mn 0.05%, Mo 0.0005%, and Zn 0.06%) was added to the water so that a trace of the blue fertilizer indicator color was visible in the water. Plants were grown for several weeks, and newly bolted plants were used in the study when the inflorescence length ranged from 2 to 10 cm. Note that during cultivation, older inflorescences were cut off at the base of their stems to stimulate growth of new inflorescence shoots. Flowering stems were thus continuously cut back over several months so that new flowering shoots could emerge for use in subsequent time-lapse studies.

Positioning the Plants for Time-Lapse

Both gravitropism and circumutation were easily observed during the POB lab period of 2 hours and 45 minutes, which allowed time to present a lab overview to the class, set up and start the study, view the movies, and have a follow-up discussion. The study was initiated when two pots of wild-type Arabidopsis plants, at the same stage of development, were placed in close enough proximity so that the inflorescent stems of both plants were clearly viewed in the cell phone/tablet viewer (Figure 1). One of the pots was placed on its side (turned 90° from the main vertical axis so that the inflorescence stems were horizontal) to initiate the gravitropic response. The other plant was left upright for viewing circumnutation.

Controlling for Light Effects Skewing the Gravitropic Response

When the light source comes from above, gravitropism is the predominant movement response in Arabidopsis plants that have been turned on their side (Kiss et al., 1997). In the light, the gravitropic response is actually enhanced (slightly) when compared to the dark (Vitha et al., 2007). Therefore, it is suitable to observe gravitropism in the light if one places a light source directly above the test plants, which will ensure that the apex of the inflorescent stems will be lifted upward in a linear vertical response. In a room with strong light coming from the side, such as a window on a sunny day, it is possible that phototropic signaling may skew the gravitropic response. In this case a curtain blocking light from the side should be used.

Making Time-Lapse Recordings

The program Lapse It was used to make recordings. A short protocol is described here:

  • Lapse It is first downloaded from lapseit.com (this step can be done prior to class).

  • For Arabidopsis, the frame interval is set to 2, and the time scale is set to 2 minutes.

  • The plants’ flowering stems are fully visible in the viewer. Support and positioning the smartphone/tablet can be done using make-shift items or purchased stands. Test-tube racks are very useful for holding phones/tablets.

  • Arabidopsis plants that are beginning to flower show the greatest displacement of the inflorescent stem position when compared to other organs. Inflorescent stem will lose flexibility with increasing maturity.

  • A piece of paper or cardboard that isn't green is used as the background. Colors that provide nice contrast are blue, purple, white, or black.

  • To initiate a recording, choose “New Capture.”

  • To begin recording, touch the red “Capture” button.

  • Avoid disturbing the setup while the recording is being made. It helps to place tape over the light switch to prevent inadvertent darkening of the background.

  • “Stop” the program.

  • Play the video to see the results.

  • Recordings are placed into the “Gallery” and need to be “Rendered.”

  • Rendered movies are then copied to “Photo Roll” and can then be downloaded or published over the web.

After 90 minutes to 2 hours and 45 minutes, students had made movies revealing dramatic movement. Links to some teaching lab movies can be seen here:

Learning Activities That Can Be Performed While Making The Recordings

While the time-lapse recordings are running, instructors can use that time to consider the purpose of movement and explore movements in other plant species. For instance, I will have students examine some “faster” moving plants, which include the “sensitive plant” (Mimosa piduca), where leaflets and leaves rapidly close when touched. Students will also examine the well-known Venus fly trap. I discuss how these plants are the “cheetahs of the plant world”—the fastest of all plants—and ask them to consider why such traits evolved. I also ask students to consider the advantages and disadvantages of rapid plant movement vs. slower movements, those of which are detectable vs. those of which are undetectable to the naked eye. The goal is to consider not only that plants move, but also that movement has a purpose in and of itself. The purpose of the movement may be clear, as in the case of carnivory or gravitropism, or be a mystery, as in the case of mimosa leaf closing or circumnutation. While the recordings are running I might show and discuss Lubkin's Figure 2 (1994), which presents a model behind the mechanics of circumnutation. In this model rotating waves of turgor pressure are shown in cells rotating around the circumference of the stem, thereby creating the rhythmic movement of circumnutation.

Preliminary Assessment of the time-lapse lab method

Upon completion of the lab sessions, an on-line qualitative assessment was conducted to gauge student's impressions of the time-lapse lab. The entire class of 425 students were queried. In total 126 students responded, of which 100 (the maximum allowed for analysis) student responses were randomly chosen and analyzed using Survey Monkey. The complete survey of five assessment questions and student responses is shown here in Table 1.

Table 1.
Five assessment questions and student responses.
Strongly DisagreeDisagreeNeutralAgreeStrongly Agree
  1. The time-lapse experiment made me more interested in learning about plants.

 
5% 11% 20% 43% 21% 
  1. Using time-lapse with my smartphone/tablet has interested me in doing my own time lapse experiments outside of class.

 
5% 19% 30% 30% 16% 
 True False    
I was inspired by the lab to perform time lapse with my smartphone/tablet. 56% 44%    
I recommend continuing with time-lapse experiments in POB Lab. 79% 21%    
I showed my time-lapse movies that I made in the POB Lab to individuals not in the POB Lab (friends, family members, etc.). 46% 54%    
Strongly DisagreeDisagreeNeutralAgreeStrongly Agree
  1. The time-lapse experiment made me more interested in learning about plants.

 
5% 11% 20% 43% 21% 
  1. Using time-lapse with my smartphone/tablet has interested me in doing my own time lapse experiments outside of class.

 
5% 19% 30% 30% 16% 
 True False    
I was inspired by the lab to perform time lapse with my smartphone/tablet. 56% 44%    
I recommend continuing with time-lapse experiments in POB Lab. 79% 21%    
I showed my time-lapse movies that I made in the POB Lab to individuals not in the POB Lab (friends, family members, etc.). 46% 54%    

The last (fifth) question is a striking indicator of student interest. Nearly half of the students took time to show their data to nonstudents, an informal form of student-to-student learning dissemination.

Conclusion

The advent of inexpensive, high-quality movie recording capabilities presents many new possibilities for time-lapse studies of plants. Until now, the use of time-lapse methods with plants has been reserved for a few scientists with expensive, sophisticated equipment. Digitization opens the window to time-lapse investigative experiments in the classroom. The speediest plant movement is typically found in the growing organs (Stolarz, 2009). In this system the tissues toward the apex of the Arabidopsis inflorescence appear to show the greatest rate of movement. With the democratization of time-lapse studies in plants, a tremendous number of species and varieties can easily be filmed at different stages of development. Already the Internet is loaded with homemade videos showing various aspects of plant development in time-lapse format.

The advantage of using Arabidopsis for teaching lab exercises is that it offers a copious number of mutants for studies to help students contextualize the role of genes in plant growth and development. Using Arabidopsis also provides an opportunity for educators to familiarize students with an important plant model system. As a well-studied model system, Arabidopsis research has led, and continues to lead, to a better understanding of how a plant interacts with and responds to its environment. However, the main advantage with Arabidopsis is that it is an exceedingly fast mover, providing vivid results within the short time available in a standard lab class. The POB lab lasts 2 hours and 45 minutes, and must accommodate up to 500 students within a week; thus a camcorder-computer set-up is impractical. Use of their own recording devices personalizes the lab and allows students to freely disseminate their findings. In this method the Arabidopsis inflorescence stem gravitropic response is completed in 90 minutes, which corresponds with published results (Fukaki et al., 1996). The use of smartphones to observe gravitropism in Arabidopsis builds upon an earlier teaching lab, which uses static images of a genetic mutant impaired in gravitropism to study the role of statoliths as internal regulators of gravitropic sensing, where students measure the curvature of roots or shoots (Kiss et al., 2000). This lab presents a useful method to demonstrate the Colodny-Went hypothesis of how statolith movement triggers auxin redistribution to mediate plant tropic responses (Williams, 2013).

In my teaching labs, students gasp in astonishment the moment they view their video recordings, as they had no idea that plants move so quickly. For longer term movement processes, students may elect to leave their devices for longer time periods, even overnight (preferably keeping them in a secure place). In reality plants are dynamic moving organisms—in some ways equivalent to animals and in many other ways rather distinct. Analysis of time-lapse recordings helps students conceptualize plant behavior. This new field of plant signaling and behavior can be used to teach plant biology from a more integrated perspective (Brenner et al., 2006), allowing students to consider the connections among environment, genes, and complex plant processes. This simple time-lapse system has set the stage for the development of software that will allow quantification of plant movement properties. This allows students to utilize this cheap and prevalent technology to decipher the purpose of some of these movement properties, such as circumnutation, which has been well known since Darwin, who carefully characterized this process in numerous species (Darwin, 1880).

To help students explore the role of movement in plants, we are developing a prototypic software program, Plant Tracer, to quantify time-lapse movies for use in both education and research. Once the app has been produced, it will be available to the general biology community at https://www.planttracer.com. One planned utility of this app will be to enable students to isolate novel mutants impaired in the gravitropic responses and in circumnutation to better understand these processes.

I would like to acknowledge Joye Wang and Angelica Guercio for their assistance in the lab. I would also like to acknowledge Dr. Yao Wang and Angelica Guercio for critical comments on portions of the text. I would also like to thank Xi Lou for sharing his lab-created video. Development of the time-lapse teaching lab was supported by NSF grant #1611885 and the NYU Curricular Development Fund.

Resources

Resources
Arabidopsis Biological Resource Center. Order Stocks: https://abrc.osu.edu/order-stocks. Seed Handling: https://abrc.osu.edu/seed-handling.
Plant Tracer Web Page. https://www.planttracer.com
SurveyMonkey Inc., San Mateo, CA. https://www.surveymonkey.com/

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